the impact of global climate change on genetic diversity...

INVITED REVIEWS AND META-ANALYSES

The impact of global climate change on genetic diversitywithin populations and species

STEFFEN U. PAULS,* CARSTEN NOWAK,*† MIKL !OS B !ALINT*‡ and MARKUS PFENNINGER*1

*Biodiversity and Climate Research Centre (BiK-F) by Senckenberg Gesellschaft f€ur Naturforschung and Goethe University,Senckenberganlage 25, D-60325, Frankfurt/Main, Germany, †Conservation Genetics Group, Senckenberg Research Institute andNatural History Museum Frankfurt, Clamecystraße 12, D-63571 Gelnhausen, Germany, ‡Molecular Biology Center,Babes-Bolyai University, Str. Treboniu Laurian 42, 400271 Cluj, Romania

Abstract

Genetic diversity provides the basic substrate for evolution, yet few studies assess theimpacts of global climate change (GCC) on intraspecific genetic variation. In this review,we highlight the importance of incorporating neutral and non-neutral genetic diversitywhen assessing the impacts of GCC, for example, in studies that aim to predict thefuture distribution and fate of a species or ecological community. Specifically, weaddress the following questions: Why study the effects of GCC on intraspecific geneticdiversity? How does GCC affect genetic diversity? How is the effect of GCC on geneticdiversity currently studied? Where is potential for future research? For each of thesequestions, we provide a general background and highlight case studies across the ani-mal, plant and microbial kingdoms. We further discuss how cryptic diversity can affectGCC assessments, how genetic diversity can be integrated into studies that aim to pre-dict species’ responses on GCC and how conservation efforts related to GCC can incor-porate and profit from inclusion of genetic diversity assessments. We argue thatstudying the fate of intraspecifc genetic diversity is an indispensable and logical ventureif we are to fully understand the consequences of GCC on biodiversity on all levels.

Keywords: cryptic species, global change biology, phylogeography, species distribution model-ling, species range projections

Received 28 July 2012; revision received 22 October 2012; accepted 25 October 2012

Introduction

Intraspecific genetic variation provides the basis for anyevolutionary change and is thus the most fundamentallevel of biodiversity (May 1994). In the light of currentglobal climate change (GCC), it is necessary to studythe effects of climatic alterations on intraspecific geneticdiversity if we are to fully understand the evolutionaryconsequences of GCC and its long-term effects on biodi-versity. However, despite an increasing number of stud-

ies examining the effects of GCC on biodiversity onspecies and community level, few studies focus on pat-terns of intraspecific genetic variation.Global climate change will impact intraspecific genetic

diversity in many ways. These include, but are not lim-ited to (i) changes in the distribution of genetic variantsin space and time as the ranges of populations and spe-cies change, (ii) changes in levels of phenotypic plasticityof individuals and populations as they respond to newenvironmental conditions, as well as (iii) evolutionaryadaptation to changing environmental conditions (Hoff-mann & Sgro 2011). In many cases, these changes willreduce genetic diversity in populations and species, inextreme situations to the point where genetic impover-ishment will contribute to reduced population viabilityand extinction.In the following review, we first address the question

why the impact of GCC on genetic diversity merits

Correspondence: Markus Pfenninger, Biocampus Siesmayer-straße, Siesmayerstraße 70B, D-60323 Frankfurt/Main,Germany, E-mail: [email protected] U. Pauls, Biodiversity and Climate Research Centre(BiK-F), Senckenberganlage 25, D-60325, Frankfurt/Main,Germany. Fax: +49 (69) 7542-1800; E-mail: [email protected] invitation to review went to M. Pfenninger.

© 2012 Blackwell Publishing Ltd

Molecular Ecology (2013) 22, 925–946 doi: 10.1111/mec.12152

scientific scrutiny. Here, we briefly outline the impor-tance of genetic diversity for species reactions to GCC,provide examples of the effects of GCC on commerciallyvaluable organisms where our basic understanding inthe field is grounded, and raise the issue of cryptic diver-sity in the context of GCC. Second, we ask how GCCimpacts intraspecific genetic diversity. In this section, weassess the importance of GCC-induced range shifts andGCC effects on the selection regime for genetic diversity.Third, we ask how scientists are currently assessing theimpact of GCC on intraspecific genetic diversity and theissues they are facing. We address the question what wecan learn from inferences about a species’ history andfrom assessments of neutral and non-neutral geneticdiversity and its interactions with the environment.Finally, we outline how we think this line of research willproceed in the future. We highlight genetic diversity asan important but previously largely neglected level ofbiodiversity that is fundamental for species adaptivecapacities. We aim to raise awareness for this shortcom-ing and encourage the global change biology communityto embrace and further the knowledge on the impactsthat GCC will have on biodiversity’s most fundamentallevel.For the purpose of this review, we define genetic

diversity as all the genetic variants within and amongpopulations of evolutionary lineages, where evolution-ary lineages can represent recognized morphospecies,morphologically cryptic species or other evolutionarysignificant units (ESUs).

Why study the effects of GCC on intraspecificgenetic diversity?

Species can react to GCC by persisting in new condi-tions through ecological plasticity or adaptation (Riddleet al. 2008; Scoble & Lowe 2010; Hoffmann & Sgro 2011)or they can avoid new conditions by shifting their habi-tat or their range (Parmesan et al. 1999; Chen et al.2011). Failure to succeed in either of these mechanismswill likely lead to population extirpation or—in theworst case—extinction of entire species (Dawson et al.2011). However, no matter which of the mentioned tra-jectories an individual population or species will takeunder GCC, all will influence the amount and distribu-tion of intraspecific genetic diversity, most often associ-ated with a loss of genetic variation. Genetic variantswith phenotypic effect are, however, the fundamentalbasis for evolutionary change and ultimately for bio-diversity as such. Genetic diversity has been shown tobe important for the fitness of individuals as high levelsof heterozygosity may increase individual fitnessbecause the effect of deleterious mutations can becounterbalanced (Chapman et al. 2009). Also, the stress

resistance of populations (Nowak et al. 2007; Markertet al. 2010) and their adaptive potential (Frankham2005) is positively associated with the degree of overallgenetic diversity, the loss of which is therefore poten-tially a threat to the affected population or species.The potential of GCC to reduce intraspecific genetic

diversity does not only have academic or conservationconsequences but pertains to the sustenance of human-ity. In general, genetic diversity has been recognized tobe important for maintaining ecosystem services, forexample, by ‘reducing pest and disease problems, andencouraging recovery from disturbance (Burton et al.1992)’. It is not by chance that most work examining theeffects of GCC on genetic diversity has focussed oncrops (e.g. rice, Negrao et al. 2008), commercially impor-tant fish (e.g. salmonids, Bryant 2009), forest trees (e.g.Parker et al. 2000) or more generally on agricultural sys-tems (Challinor et al. 2009). In crop sciences, it is nowrecognized that by focussing on specialized breed lines,the potential of crops to adapt to GCC is limited andthat biosynthetic pathways are likely to be lost, limitingthe potential nutrient value of crop plants (Reynolds &Borlaug 2006; Burlingame et al. 2009). In response tothese threats, ideas have begun circulating to inbreedold cultivars (e.g. Charmet 2011) to maintain and pre-serve landraces for sustaining adaptive potential in agri-cultural resources (Newton et al. 2010), in an efforttermed the ‘doubly green revolution’ (Reynolds &Borlaug 2006). These approaches have also been adaptedin the forest industry: Aravanopoulos (2010) proposesusing Mediterranean stocks of fast-growing, economi-cally sought tree species to genetically diversify north-ern forests with tree clones that were selected underhigher temperature or drier conditions. The impact ofGCC on agriculturally important species is likely to beexacerbated by inbreeding due to human harvesting (Ci-brian-Jaramillo et al. 2009). Increased anthropogenicfragmentation of populations of both economicallyimportant and other species that limits gene flow mayalso leave populations that are locally adapted to cur-rent conditions, but maladapted to future conditionsunder GCC, at peril of increased stress (Davis & Shaw2001; Jump & Penuelas 2005; Hof et al. 2011a).Ongoing GCC also impacts the genetic diversity of spe-

cies that are not studied nearly as well as most economi-cally relevant organisms. For these species, an additionalissue arises from the fact that taxonomically recognizedmorphospecies are often not the evolutionary, ecologi-cally or even economically relevant units. The ubiquitouspresence of cryptic species or ESUs (Pfenninger & Sch-wenk 2007) suggests that morphospecies-based approa-ches may seriously underestimate GCC effects onbiodiversity (see Box 1). In a recent study, for example,B!alint et al. (2011) showed that without acknowledging


926 S . U. PAULS ET AL.

intraspecific genetic variation and cryptic diversity, GCCeffects are likely to be drastically underestimated.Despite the obvious shortcomings of morphospecies level

assessments, subspecific genetic diversity has not yetreceived much of its deserved attention in the biodiversityand climate change discussion (e.g. Bellard et al. 2012).

Box 1 How does cryptic diversity affect GCC projections?

Cryptic diversity is a common phenomenon and has become a focus of biodiversity research following (i) method-ological advances in integrated taxonomy (Wheeler 2004, 2008; Dayrat 2005; Padial et al. 2010), DNA taxonomy(Vogler & Monaghan 2007), DNA barcoding (Hebert et al. 2003) and (ii) a general increase in biodiversity studiesthat apply molecular tools. In particular, widespread species with broader ecological niches are often taxonomicallycomplex entities that represent numerous subspecies or other cryptic diversity units (Callaghan et al. 2004; Ujv!arosiet al. 2010). Cryptic diversity may complicate assessments of GCC effects on biodiversity in a number of ways.First, cryptic species or cryptic lineages can follow independent evolutionary trajectories, that is, they representindependent ESUs and may thus show different responses to GCC (Davis & Shaw 2001; Galbreath et al. 2010; Heu-ertz et al. 2010). In addition, taxa that in the past evolved high levels of genetic diversity or multiple ESUs associ-ated with varying environmental conditions may be more likely to do this again in the future (Callaghan et al.2004). However, the rate of ongoing GCC may be quicker than major historic environmental changes, and this lim-its the amount of time for evolutionary responses (but see Steffensen et al. 2008 and Hof et al. 2011b). Additionalanthropogenic pressures like habitat fragmentation may further impact species responses. Nonetheless, the fate ofindependent cryptic lineages or ESUs can vary under different GCC scenarios (B!alint et al. 2011; Habel et al. 2011)and may be very different from the assessment for a morphospecies as a whole (B!alint et al. 2011; Taubmann et al.2011; Fig. 1).Second, cryptic diversity complicates palaeoreconstructions: cryptic species with different ecological niches or envi-ronmental change responses are necessarily considered as one unit in these reconstructions (Bauch et al. 2003). Thiswill compromise the use of palaeontological data to infer historic reactions to environmental change and the use ofthese inferences to inform future predictions on GCC responses. Ancient DNA approaches may provide a solutionfor identifying cryptic diversity with the palaeorecords of select taxa (Magyari et al. 2011).Third, due to the omnipresence of cryptic diversity and the individualistic responses of ESUs to environmentalchange, community diversity comparisons and assessments based on morphospecies are oversimplistic and mayeven lead to inefficient conservation practices (Fayle et al. 2011; see Box 2). Because cryptic species and cryptic lin-eages are more or less evenly distributed among major metazoan taxa and biogeographical regions (Pfenninger &Schwenk 2007), these difficulties should generally be taken into account in studies aiming at assessing GCC effectson species or communities. Several different analytical tools and approaches facilitate assessments of cryptic diver-sity within a given sample (e.g. Ratnasingham & Hebert 2007; Monaghan et al. 2009). Expanding on the approachused in B!alint et al. (2011), Pfenninger et al. (2012) suggest a methodological approach to make GCC inferencesbased on ESUs that assess the adequacy of sampling depth at different organizational levels of intraspecific geneticdiversity (haplotypes, ESUs, species; see Box 3).

How does GCC affect genetic diversity?

We extracted two fundamental but not mutually exclu-sive processes by which GCCmay affect genetic diversity:(i) change in the geographical location and extent of therange and (ii) changes in the local selection regime. Bothprocesses are predicted to have specific effects on thegenetic make-up, which we will address in turn.

Genetic consequences of range shifts

Effects at the edge of ranges. Range shifts are usually thecombined effect of the colonization of newly emergingsuitable habitat coinciding with the migration and thenextinction in areas that have become unsuitable. The

effects of range shifts on neutral genetic diversity haverecently been subject of numerous simulation studiesthat advanced our understanding on how these parame-ters influence the temporal and spatial patterns of neu-tral genetic diversity under range shift scenarios.Cobben et al. (2011), McInerny et al. (2009) and Arenaset al. (2012) show that the leading edge of a shiftingrange under GCC has low levels of neutral geneticdiversity. This is caused by recurring founder effects,allele surfing and because only a part of the originalgenetic variation moves to a newly colonized habitat.While the leading edge of a shifting population oftencomprises low levels of genetic variation, McInerny et al.(2009) show that the leading edge is also the source formost of the surviving lineages and persisting alleles,


GENETIC DIVERSITY LOSSES UNDER CLIMATE CHANGE 927

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Median vector

Extant/persisting and lost GMYC species

Extant/persisting and lost mtCOI haplotype,color-coded by regionConnection among extent/persisting and losthaplotypes/median vectors

color-coding of regions:

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while trailing edge lineages and alleles are more likelyto go extinct. Under otherwise unchanged conditions,range contractions should lead to decreases in effectivepopulation size and in extreme cases to population bot-tlenecks that may reduce genetic diversity of popula-tions (e.g. O’Brien et al. 1987; Hewitt 1996; Luikart et al.1998). In a simulation study, Arenas et al. (2012) explic-itly test the effects of range contractions under differentmodels of dispersal directed either towards a potentialrefuge or equally in all directions. In their simulations,the speed of range contraction was very important.Somewhat counter-intuitively they show that slow-rangecontractions can lead to greater losses of overall geneticdiversity than fast-range contractions. Under fast-rangecontractions, initial levels of genetic diversity are betterpreserved, because slower-range contractions are accom-panied by more coalescence events and ultimately indi-viduals sampled from the surviving refugia are morelikely to share common ancestors.Strong selection pressure may act on the leading edge

of an expanding population, for example, on dispersalcapacity or host selection in insects (Hill et al. 2011). In aselective sweep, newly advantageous alleles as well asthe linked neutral alleles become fixed in the affectedsubpopulation, population or species, thus reducinglocal genetic diversity. Another process by which localgenetic drift can cause reduced genetic diversity in theleading edge of an expanding population is ‘surfing’(reviewed by Excoffier & Ray 2008). Allele surfingdefines the situation when an allele becomes over-proportionally frequent at the expanding front throughgenetic drift. The pattern resulting from this processmay be indistinguishable from that of a selective sweep,although the underlying process without selection isvastly different and requires a different evolutionaryinterpretation (Excoffier et al. 2009). In a rare empiricalstudy on allele surfing, Hallatschek et al. (2007) use twofluorescently marked strains of Escherishia coli (Migula1895) to demonstrate that surfing leads to severe changesin the neutral variation of natural populations. Geneticpopulation structure also changed because individualalleles dominated certain regions of newly invaded terri-tory, without these alleles being under selection. It

appears that range expansion may lead to complexpatterns of population genetic structure with regions oflow genetic diversity separated by sharp gradients inallele frequency of individual loci and that these patternscan arise without the influence of rare long-distance dis-persal events. However, this structure is likely to erodeover time due to gene flow between contact zones of dif-ferent adjacent regions (Excoffier & Ray 2008).These theoretically derived predictions have important

consequences for expectations of the genetic make-upof populations under GCC conditions if species respondthrough range shifts. First, all studies show that rangeshifts should lead to reduced overall genetic variation.Second, rear-edge populations of species postglaciallyrecolonizing central and northern Europe from southernrefugia have been shown to harbour large proportionsof genetic diversity and ancestral lineages. Thus, theserear-edge populations play an important role in main-taining long-term genetic diversity in these species(Hampe & Petit 2005). Based on the simulation studies,these lineages appear particularly threatened and maydeserve particular attention in conservation (see Box 2).

Effects within the range. Besides the location of a (sub)population within a shifting range (leading edge, centreor rear-edge), simulation studies conclude that neutralgenetic diversity of populations decreases withincreased short-term regional climate variation (Cobbenet al. 2011) and with increasing speed of the range shift(Arenas et al. 2012). Some recent empirical studies haveused simple models to project losses of genetic diversityassociated with range shifts (Sork et al. 2010; B!alint et al.2011; Collevatti et al. 2011; Habel et al. 2011; Taubmannet al. 2011; Alsos et al. 2012). While these are pioneeringstudies in addressing the effects of GCC on the distribu-tion and projected losses of intraspecific genetic varia-tion, they suffer from relatively simple dispersal models,do not account for adaptation and have with the excep-tion of Sork et al. (2010) not implemented measures ofshort-term regional climate variation. Empirical studieson population structure also made inferences on theeffects of range shifts on the distribution of geneticdiversity (Campos et al. 2010; Pfenninger et al. 2011;

Fig. 1 Schematic figure of projected genetic diversity losses of the caddisfly Drusus discolor. Shown is the mtCOI haplotype diversityfrom the range-wide sampling of D. discolor in the median joining network (left column). Coloured circles represent haplotypes;colour coding indicates regional origin of the specimen carrying a specific haplotype; and haplotype diameter is scaled to the numberof individuals carrying a specific haplotype. Lines between haplotypes indicate connections; connections are not scaled to geneticdistance; and median vectors connect lineages. Species delimited using a general mixed Yule coalescent model (GMYC species,Monaghan et al. 2009) are grouped by shaded shapes. Grey shapes indicate current or persisting GMYC species; orange shapes indi-cate GMYC species projected to be lost under the respective IPCC CO2 emissions scenario. The right column shows models of theclimatically suitable areas for D. discolor in the present (top) and 2080 under the B2a CO2 emissions scenario (middle) and A2a CO2

emissions scenario (bottom). White circles show localities used to derive the climatically suitable areas and haplotype distribution.Data from Pauls et al. 2006 and Balint et al. 2011.



B!alint et al. 2012). Besides causing reductions in overallgenetic diversity, range expansions, range contractionsand range shifts indeed altered the distribution ofgenetic diversity across the range (e.g. Excoffier et al.2009; Sork et al. 2010; Pfenninger et al. 2011; Arenas et al.2012). Sork et al. (2010) show that GCC response amongregional populations of California valley oak may be dif-ferent and lead to varying patterns in the future distri-bution of genetic variants. This means that theimportance of adaptation, migration and tolerance asGCC responses will vary in different parts of the species

range. Yang et al. (2011) observed shifts in intraspecificgenetic diversity within an alpine chipmunks’unchanged range, highlighting the fact that interpreta-tions of observed spatial migration at the species levelmay not account for more subtle subspecific GCCresponses. Following up this work, Rubidge et al. (2012)show how GCC-induced range reductions of one alpinechipmunk species in California resulted in patterns ofgenetic erosion through time, while a congeneric speciesshowed no signs of range reduction, range shift orgenetic erosion.

Box 2 Conservation of genetic diversity under global climate change

Technical advances in the field of molecular genetics along with the rising importance and public awareness of nat-ure conservation issues have led to the rise of ‘conservation genetics’ over the past two decades (e.g. DeSalle &Amato 2004). Examples for the successful application of molecular markers in conservation research and popula-tion management are manifold and include the estimation of genetic diversity loss and grades of inbreeding (e.g.Marsden et al. 2012), correct species assignment (e.g. Rach et al. 2008), population monitoring (Schwartz et al. 2007),delineation of conservation units (Fraser & Bernatchez 2001), revealing introgression from domestic forms into wildpopulations (Randi 2008) and tracking the success of invasive species (e.g. Dlugosch & Parker 2008) or re-intro-duced populations (e.g. De Barba et al. 2010). In a world of rapid environmental change, such as ongoing GCC,genetic diversity within and between populations undoubtedly becomes increasingly important, as it allowspopulations to adapt to environmental change and might enhance stress resistance of populations (see text fordetails). With this in mind, we suggest three areas where incorporation of genetic diversity measures inGCC-related species conservation strategies are particularly important:

1 Population management for critically endangered populations, for which genetic diversity loss and inbreedingmight pose direct and severe concerns. The use of high-resolution marker sets covering large parts of the gen-ome seems most appropriate for this purpose. Direct measures of inbreeding depression, however, do requireexperimental approaches, which are hardly ever applicable for the species of interest. The finding that inbreedingdepression is enhanced under environmental stress (Armbruster & Reed 2005), including temperature stress, hasparticular relevance under GCC conditions and needs to be implemented in population viability analyses.

2 Assignment of populations and regions with particular conservation value under GCC species distribution models(SDM) are quite commonly used in conservation efforts to assess the potential of certain areas as reserves for targetspecies or communities under GCC (e.g. Ponce-Reyes et al. 2012). Recent studies suggest using SDM alongsidegenetic assessments to project potential diversity losses under GCC (e.g. Scoble & Lowe 2010; B!alint et al. 2011; Ha-bel et al. 2011; Taubmann et al. 2011; Alsos et al. 2012; Pfenninger et al. 2012). Combining these data will allow prior-itizing populations and regions for conservation, allowing for an optimized balancing between future survivalprobabilities and preservation of evolutionary potential. This strategy requires sound measures of genetic diversityas suggested by Pfenninger et al. (2012) and will be most effective on large (area-wide) scales and among genetic lin-eages with independent evolutionary histories (e.g. ESUs).

3 Estimating dispersal capacities is not directly related to the conservation of genetic diversity itself. However, theability to disperse is of crucial importance for organisms to track shifting climatic niches under GCC. Currently,the unknown dispersal abilities of species are considered one of the blind spots of current attempts to projectGCC effects on biodiversity (Engler et al. 2009) and also limit conservation efforts more generally (Smith & Green2005). The use of fine-scale genetic analyses, for example, by microsatellites or single nucleotide polymorphisms(SNP) panels and methodological approaches implemented in the emerging field of landscape genetics (Manelet al. 2003) promises to provide crucially needed data not only to identify dispersal events, but more importantlyto reveal the extent of gene flow in time and space.

A way by which GCC and range shifts may enhancelevels of genetic diversity apart from increasing overallmutation rate is the modification of reproductive isolation

among lineages and species (Hoffmann & Sgro 2011).Phylogeographic studies have provided ample evidencethat postglacial climate shifts triggered expansions and



migrations that brought previously isolated lineages intosecondary contact, thereby mutually increasing localgenetic diversity (e.g. Hewitt 2000; Pfenninger & Posada2002; Pauls et al. 2006, 2009). Disturbance regimes in gen-eral can lead to hybridization among isolated genetic lin-eages (Pfennig 2007; Schwenk et al. 2008), and postglacialsecondary contact has also led to climate-driven hybrid-ization events in several species. Hailer et al. (2012), forexample, showed that polar bears (Ursus maritimus Phi-pps 1774) display high similarity to brown bears (Ursusarctos Linnaeus 1758) in mtDNA sequences, but not innuclear genes. This is best explained by a ‘mitochondrialcapture’ event of brown bear mtDNA during past phasesof warm climates, which reduced the effective size of thepolar bear population and facilitated introgression ofgenetic material. Similar patterns are known for otherspecies as well, for example, hares (Melo-Ferreira et al.2005) and butterflies (Zakharov et al. 2009). It wasrecently also shown that specific weather conditions weredriving hybridization rates in two butterflies species (Jah-ner et al. 2012), suggesting a great potential of GCC tomodify species boundaries. Supporting evidence forincreased introgression by hybridization under GCC con-ditions comes from the copepod Tigriopus californicus(Baker, 1912), where hybrid breakdown was less severeunder thermal stress (Willett 2012). However, also thecontrary was observed in parasitic wasps (Koevoets et al.2012), stressing the idiosyncratic ways in which GCC willaffect individual systems.

Genetic consequences of GCC on the selection regime

Variations in micro-evolutionary responses. Populationsmay face changing environmental conditions withoutdirectly responding through habitat or range shifts.Recent studies indicate that the genetic diversity ofstationary populations may also be affected by GCC. Aspecies’ ability to cope with changed conditions dependson the evolutionary adaptive capacity (Riddle et al.2008) via micro-evolution, for example, selection forlocal genotypes better adapted to changing environmen-tal conditions, but also including the evolution ofpheno-typic plasticity (Canale & Henry 2010; Hoffmann& Sgro 2011). Adaptive micro-evolutionary processesrely on sufficient genetic variation upon which naturalselection can act (Hoffmann & Sgro 2011) and the estab-lishment probability of beneficial mutations (Peischel &Kirkpatrick 2012). Under a deteriorating environment,such as GCC represents for many species, adaptivemicro-evolutionary processes will tend to reduce geneticvariation at the selected loci and, more importantly, inthose parts of the genome that are hitchhiking with it(Via & West 2008; Via 2009). As Charlesworth et al.(1997) could show, this hitchhiking process affects larger

parts of the genome the smaller the population is. There-fore, fast increase in and multiple levels of environmen-tal stress can strip a population of most of its geneticvariability as it adapts to them, reducing the possibilityto react to future selective challenges. A series of labora-tory experiments on nonbiting midges suggested thatexposure to a stressor over a few generations can indeedlower neutral genetic diversity by adaptation as well asenhanced genetic drift (Vogt et al. 2007; Nowak et al.2009) and diminish the possibility to adapt to a second-ary stressor (Vogt et al. 2010).As does genetic variation, adaptation potential varies

across a species’ populations and its range (Davis &Shaw 2001; Eckert et al. 2008). It is thus likely that indi-vidual populations within a species will react differ-ently to GCC (e.g. Procaccini et al. 2007), especially ifthere are stronger selective pressures in different partsof the range or changes in selection pressure (Hoffmann& Sgro 2011), for example, to stronger temperaturechanges in certain parts of a range (e.g. Jensen et al.2008), to accelerated range expansion in leading edgepopulations (e.g. Hill et al. 2011), or to stronger compe-tition through climate amelioration in the centre of therange of Arctic species (e.g. Callaghan et al. 2004). Goodexamples of this are many invasive species that adaptvery rapidly to new selective pressures in the non-native ranges (Sax et al. 2007). Also, two recent studieshave highlighted that different geographical accessionsof the model species Arabidopsis thaliana (L.) Heynh.1841 are locally adapted to climate conditions and showthat relative fitness is linked to specific climate-adaptedgenetic loci (Fournier-Level et al. 2011; Hancock et al.2011). Such differential adaptations to the same or dif-ferent selective pressures may even foster reproductiveisolation (Schluter 2001; Via 2012).

The speed of ongoing GCC and effects of increased climatevariation. The speed of adaptation is an important com-ponent in GCC and is related to the strength of selec-tive pressures on a population or species, the rate withwhich these selective pressures change and the adaptivepotential of populations and species (Hoffmann & Sgro2011). Trees, for example, are rather long-lived in rela-tion to the speed of current GCC. However, the highlevels of genetic diversity and large effective populationsizes of many tree species greatly increase their chancesof adapting within a few generations (Petit & Hampe2006). On the other hand, the current rate of GCC is sorapid—though not unprecedented in recent geologichistory (Steffensen et al. 2008; Hof et al. 2011b; T!othet al. 2011)—that the resulting strong selection pressuresmay rapidly distance populations from the environmen-tal conditions to which they are locally adapted andpromote local extirpation (Davis & Shaw 2001), even in



trees (Kramer et al. 2008). Even in cases of the recentgeologic history when a forest is able to respond torapid climate change with fast horizontal range shifts(e.g. Magyari et al. 2012), ancient DNA sequences con-nect plausible decreases in genetic diversity of a treepopulation to Holocene climatic oscillations (Magyariet al. 2011).Most GCC-related research has focused on changes in

climatic means, for example, warming temperature orgeneral changes in annual precipitation. While changesin mean climate conditions are likely to cause losses ingenetic diversity in many species, increases resultingfrom GCC are also plausible. Higher temperatures, forexample, will generally increase metabolism in themajority of species, and this is linked with increasedmutation rates (Muller 1928; Davis et al. 2005; Stegenet al. 2009; but see Held 2001). It remains unclear, how-ever, if increased mutation rates could in turn add sig-nificantly to standing functional variability (Garcia et al.2010; McGaughran & Holland 2010). Increased climatevariation could also have major effect on genetic diver-sity, but its effects have rarely been studied. Increasesin climate variation are expected for both precipitationpatterns as well as temperature conditions (Karl et al.1995; Christensen et al. 2007). Because any shift inselection regime is likely to change the frequency distri-bution of the responsive alleles in populations, bothkinds of increases in short-term climatic variation havethe potential to affect populations [e.g. changes inpopulation growth rates (Drake 2005)] and individuals[e.g. changes in an individuals’ phenotypic plasticity-like intra-annual changes in individual growth rates(e.g. Nussey et al. 2005)].In a rare empirical case study, Avolio et al. (2012)

show that diversity in genotypes of a dominant prairiegrass species declined significantly following 10 yearsof increased intra-annual variation in precipitation.While genotype diversity decreased, the authorsobserved decreases in genotype similarity within exper-imental plots, suggesting a local increase in geneticdiversity. Thus, the response pattern is complex, andthe authors attribute this to changes in local selectionregime in the system: increased variation in precipita-tion leads to greater temporal and spatial variation insoil moisture conditions within the experimental plots.This drives differential selection in different parts of theexperimental plots in a first step towards niche differen-tiation. Avolio et al. (2012) conclude that in populationswhere initial genetic variation is sufficiently high,increased climate variation can lead to increased localgenetic differentiation via differential selection and ulti-mately to niche differentiation. Overall, however,genetic diversity will at best remain constant in the spe-cies as none of the above processes creates new genetic

variants but rather favours local shifts of allele fre-quency and the persistence of immigrating alleles.We argue that increasing climate variability can gen-

erally lead to changes in the selection regime that cancause either increases or decreases in local geneticdiversity. Under conditions of increased temperatureextremes or increased frequency of severe precipitationevents, directional selection on dispersal traits couldshift towards better dispersing capabilities to help pop-ulations avoid more frequent extreme weather condi-tions. This can change the distribution of geneticdiversity by (i) decreasing effects of genetic drift bymeans of increased gene flow, thus homogenizinggenetic diversity across space or (ii) increasing abun-dance of rare genotypes with particularly good dis-persal abilities. However, empirical studies have shownthat the relationship between habitat stability and dis-persal is not clear-cut and that positive selection on dis-persal abilities mainly occurs under conditions withpredictable environmental changes (reviewed by Ronce2007; see also Box 2). When conditions are unpredict-able, mechanisms of reduced local competition andlocal extinction probabilities complicate the situation(Ronce 2007).Increased climate variation can provide strong selec-

tion pressure on traits that are related to increased phe-notypic plasticity as organisms need to adapt to a lesspredictable environment. In a study on phenotypicdiversity in great tits (Parus major Linnaeus 1758),Nussey et al. (2005) show that there is selection towardsincreased plasticity regarding their breeding time. Phe-notypic plasticity in breeding time is heritable, and phe-notypes with low plasticity in breeding times areselected against because anthropogenic environmentalchange, including GCC, has led to phenological mis-matches between the birds and their caterpillar foodresources.

The effect of multiple anthropogenic stressors. While micro-evolutionary adaptation affects specific, functionally rel-evant parts of the genome, natural and anthropogenicstress, for example, parasites, environmental pollution,habitat perturbation or habitat fragmentation can alsolead to unspecific reductions in effective population sizeby diminishing census population size, distorting sexratios, reducing fecundity rates and increasing mortality(Lande 1988; Reed 2005) and thus additionally reducinggenetic diversity by increased drift and inbreeding(Nowak et al. 2009). The impacts of stressors are gener-ally augmented in situations where human habitat frag-mentation limits gene flow among subpopulations(Frankham 1995; but see Cobben et al. 2011). Such mul-tiple stressor conditions can initiate an extinction vortex(Gilpin & Soul!e 1986; Fagan & Holmes 2006) where



decreasing genetic diversity itself leads to decreasedstress resistance. Ultimately, populations may becomestrongly inbred, causing dramatic increases in stresssensitivity and thus enhanced extinction risk. Althoughthe effects discussed above are probably not a compre-hensive account of all possible effects of GCC ongenetic diversity, it is clear that the overall level ofgenetic diversity will likely drop in many populationsand species affected by GCC even if their range anddemography may appear unaltered (e.g. Yang et al.2011).

How is the effect of GCC on genetic diversitycurrently studied?

The potential effects of GCC on species and both neu-tral and non-neutral genetic diversity have been studiedat various scales albeit rarely as the explicit goal of therespective studies. Some studies have used range-wideor large-scale inferences of species historic responses toclimate change [e.g. based on population genetic struc-ture (Jay et al. 2012) or phylogeographic data and infer-ences (e.g. B!alint et al. 2011)] to indirectly infer potentialfuture responses to GCC or dispersal potential underGCC. In a more direct approach, ancient DNA studieshave inferred the genetic effects of relatively recent cli-mate change during the Holocene or late Pleistocene onintraspecific genetic diversity (e.g. Magyari et al. 2011).Another focus has been placed on directly linkingfunctional genetic diversity with local climate adapta-tion, albeit primarily in model species for which gen-ome-level resources were readily available (e.g.Hancock et al. 2011 and Fournier-Level et al. 2011 forA. thaliana). Since the development and rapid prolifera-tion of SDM, these have sometimes been integratedwith genetic diversity data to examine historic speciesresponses (e.g. Richards et al. 2007; Cordellier & Pfenn-inger 2009; Theissinger et al. 2011). Most work, how-ever, has been focussed on experimental studies witheconomically relevant organisms or model species. Wediscuss these approaches in turn below.

Can the past inform the future?

Insights on historic range shifts and historic distributions ofgenetic diversity. Most phylogeographic studies that dis-entangle population history during the Pleistocene andthrough the Holocene warming implicitly reconstructthe fate of genetic diversity during a major GCC (Avise1998). Phylogeographic data sets inform how speciesreacted to GCC in the past, for example, by providinginformation on routes and time frame of the (re)coloni-zation of the present range, long-term migration barri-ers, location of hybrid or suture zones, location of

refugia, and/or temporal niche conservatism (Schmitt2007; Scoble & Lowe 2010). Dispersal and migrationmechanisms, in particular, have been one focus of infer-ence for historic GCC responses based on phylogeo-graphic data (e.g. Taberlet et al. 1998; Hewitt 1999;Abbott et al. 2000; Pfenninger & Posada 2002; Schmitt2007; Engelhardt et al. 2011). Intuitively, it is clear thatsedentary species have a disadvantage compared tomobile species in tracking suitable habitat conditionsunder GCC by means of migration (Callaghan et al.2004). However, this drawback may be at least partiallyset off by passive dispersal (e.g. Bilton et al. 2001) orrare long-distance dispersal events (Nathan 2006).Another focus of phylogeographic inference has been

on locating refugia. This is important for predicting spe-cies responses to GCC for two reasons. First, knowingthe location of refugia is important for assessing thescale and tempo of past migrations and range shifts ofspecies in response to past GCC (e.g. Birks & Willis2008; Petit et al. 2008). For example, it is clear from fos-sil data that small populations of many plant specieshave survived in favourable microhabitats (microrefu-gia) embedded within large unsuitable areas duringperiods of rapid climate cooling. These acted as sourcepopulations during subsequent warming (Birks & Willis2008; Feurdean et al. 2012). Second, locating refugia canhelp us characterize the distribution of genetic diversitythrough space and time (e.g. Hewitt 1996), in particular,because refugia are often associated with higher levelsof genetic diversity (Petit & Hampe 2006). The compari-son of refugia to expansion areas may thus give anindication of how long it takes to build up predistur-bance levels of genetic diversity. The fact that expansionareas can in many cases still be distinguished from lastglacial maximum (LGM) refugial areas by their relativelack of genetic diversity is not a very encouraging pros-pect for the effect of the range shifts to come. At smal-ler scales, landscape genetic or demographic inferencescan be used to identify habitats acting as barriers orcorridors of gene flow, habitat characteristics of sourceand sink populations and locations of increased adap-tive potential (Scoble & Lowe 2010; Hoffmann & Sgro2011). All of these aspects can provide importantinsights into assessing species reactions to future GCC,for example, how likely a species is to reach itsprojected future habitat under GCC conditions basedon it past and present dispersal dynamics. An overallassessment of the adaptive capacity may be gained byestimations of how conserved environmental niches areand where areas of increased genetic diversity andlikely increased adaptive potential are located. It is thusrecognized that information on historic GCC reactionscan be used to help making predictions about speciesfuture reactions (MacDonald et al. 2008; de Bruyn et al.



2011) and examples have been published for terrestrialsnails (Depraz et al. 2008) or Arctic marine mammals(O’Corry-Crowe 2008).

Integrating phylogeography and palaeoecological data forimproved inference. Inferences about potential futurereactions can be improved when they are not based onphylogeographic data alone, but wherever possible alsointegrate palaeontological proxy data (Dawson et al.2011; but see Box 1 for problems in palaeontologicaldata arising through cryptic diversity). Petit et al. (2008)show that some tree species persisted through periodsof rapid environmental change that may be comparablein timescale to expected GCC in the 21st century. Theirmolecular data provide insights on the population levelprocesses, in particular founder effects, bottlenecks, andmigration patterns of individual intraspecific lineages.These processes would not have been uncovered by fos-sil data alone. However, the possible extinction of 89tree genera during the Pleistocene can only be recog-nized through integrating palaeontological data. Thelocal extinction of trees in Europe suggests that whilesome species persisted under severe conditions in theclimatically dynamic Pleistocene in Europe, for exam-ple, in Fennoscandian Nunataks (Parducci et al. 2012),most did not (Petit et al. 2008).Besides mobility, the above study on glacial tree per-

sistence (Petit et al. 2008) raises the importance of time-scale of environmental change. Under the current rapidrates of GCC, migration responses inferred from phy-logeographic data sets may need to be reassessed forshorter timescales (years to decades rather than decadesto centuries or millennia; Callaghan et al. 2004). Oneissue is whether the selected molecular loci are suffi-ciently responsive to rapid climate change and whethergenetic signals in the examined loci remain detectableover time (Parducci et al. 2012). However, there is alsoevidence for very rapid historic climate change (VanMeerbeeck et al. 2009), and it is debatable whetherspecies are currently facing more rapid GCC than in thepast (Hof et al. 2011b). Based on our current knowledgeon population displacement rates observed from actualrange shifts over the last few decades (Chen et al. 2011)or inferred from molecular data (e.g. Petit et al. 2008),many species are unlikely to migrate fast enough tosuccessfully track their habitats (Petit et al. 2008; B!alintet al. 2011). Whether these species will increase theirmigration rates, disperse by rare stochastic long-distancedispersal events (Nathan 2006), persist in small popula-tions in suitable microrefugia or respond throughtoleration mechanisms remains to be seen.

Phylogeography and niche conservatism. Phylogeographicinference is also often used to assess temporal niche

conservatism within species and whether or not popula-tions or species adapted to past environmental change(Callaghan et al. 2004). Comparative phylogeographicstudies have shown that responses to past GCC canvary dramatically between closely related taxa(e.g. marine gastropods: Marko 2004; land snails: Pfenn-inger et al. 2007) or between species with similar present-day habitat preferences and ecologies (e.g. montaneaquatic insects: Lehrian et al. 2009, 2010; Theissingeret al. 2011, 2012). Responses seem to be individualisticand specific for each examined taxon, which is not apromising prospect concerning the transferability ofresults among species. In some cases, responsesalso seem to vary at the intraspecific level, for example,between ESUs within a nominal morphospecies(e.g. Pauls et al. 2006; Theissinger et al. 2011). Nonethe-less, inferences based on the past allow studying ratesof biodiversity response to climate change and ecologi-cal resilience of individual species to climate change(Willis et al. 2010). As we begin to take the niche intoaccount in assessing potential impacts of GCC, it isbecoming clear that ecological or functional niches areoften not conserved the way we assume (e.g. Pfennin-ger et al. 2007; Engelhardt et al. 2011; Yang et al. 2011)and that plasticity, rapid adaptations or complex eco-logical interactions will greatly complicate projectionsof future GCC effects unless we better understand thesefactors. This is particularly true for assessments thatintegrate SDM based on climatic niche, as shown bystudies of invasive species that often successfullyinvade regions with climatic niches different from theirnative range (Sax et al. 2007).

What can we learn from integrating speciesdistributions and range projections?

Species distribution models are widely used to projectfuture suitable conditions for species, albeit with somemajor underlying assumptions (niche conservatism,modelling of relevant variables, mostly ignoring speciesinteractions), and methodological limitations dependingon the approach used. We do not discuss these here, asthey were recently reviewed by Ara!ujo & Peterson(2012). Integrating evolutionary aspects bears greatpotential for inferences on the effects of GCC on biodiver-sity and predictions on species distributions (Hoffmann& Sgro 2011). Scoble & Lowe (2010), for example, make acase for integrating intraspecific genetic diversity data inthe form of phylogeographic and landscape genetic datainto SDM. Several recent studies have implemented SDMand future predictions of climatically suitable ranges inneutral genetic diversity assessment of nonmodel organ-isms (B!alint et al. 2011 and Taubmann et al. 2011 formontane aquatic insects; Habel et al. 2011 for butterflies;



Sork et al. 2010 and Alsos et al. 2012 for plants). Threemethodological issues are common to all these studiesthat were recently addressed by Pfenninger et al. (2012):Is the sampling of genetic variation sufficient to makereliable assessments on projected allele losses? Is the

genetic diversity level that is assessed relevant for evolu-tionary processes? Is the scale of SDM projections suit-able for the sampling density of genetic diversityestimates in the study? See Box 3 for a framework toaddress these issues.

Box 3 What is the best level of genetic diversity and geographical scale for assessing GCC effects in my data set?

While research on the impact of GCC on ecosystems and species is flourishing, a fundamental component of biodi-versity—genetic variation—has not yet received its due attention in this regard. The studies that have attempted toconsider cryptic diversity when investigated the impact of GCC share some common limitations that restricts theirinformation potential. First, it is not clear at which genetic level assessments should take place (e.g. haplotypes, dif-ferent groups of haplotypes) and whether the considered level of genetic variation has been sufficiently sampled interms of diversity and spatial scale. Second, the resolution of modelling projections should be fitted to the level ofgenetic information and sampling that is being assessed (i.e. projections with high spatial resolution may be suit-able for studies with a high-resolution sampling, while the resolution of projections should be comparably lower incases where the sampling is coarse). Pfenninger et al. (2012) suggest a methodological framework for projecting theloss of intraspecific genetic diversity under GCC (Fig. 2). The approach makes use of existing techniques like hier-archical genetic clustering methods, species accumulation curves (SAC) and SDM. Their approach begins withassessing the appropriate level of genetic variation for projecting the impact of GCC on genetic diversity. The ratio-nale here is that the highest resolution of intraspecific variation that can be sampled depends on the marker systemused and that it is impossible to account for all genetic variants occurring in natural populations at this level.Additionally, an individual genotype or haplotype is likely to be irrelevant in evolutionary terms for populationsand species. In contrast to individual genotypes and haplotypes, higher levels of intraspecific genetic variants [e.g.ESUs (B!alint et al. 2011), GMYC species (Monaghan et al. 2009) or hierarchically nested clade levels (Pfenningeret al. 2012)] (i) can be exhaustively sampled and (ii) most importantly are more likely to be relevant for the evolu-tion of a population or species. The next step is to assess the completeness of genetic sampling at the chosen levelof inference using SAC at the level of genetic units. The third step is to choose the appropriate scale of spatialinference for genetic diversity loss prediction. This is defined by the geographical resolution at which the samplingof the genetic diversity is comprehensive or complete and may be found by an iterative process that comprisesusing increasingly higher levels of genetic diversity, the resampling of the regions of interest, reducing the resolu-tion of SDM projections or any combination of these. The final step is to make projections of range losses and asso-ciated losses of genetic diversity based on the genetic and geographical scales that have been sufficiently sampled(Fig. 2). The suggested approach presents a feasible method to tap the rich resources of existing phylogeographicdata sets and guide the design and analysis of studies explicitly designed to estimate the impact of GCC on a cur-rently still neglected level of biodiversity.

More generally, when making inferences about thefuture using SDM projections, we generally assumetemporal niche conservatism. Callaghan et al. (2004)reviewed how estimations of current gene flow andspecies mobility compared with inferences about his-toric migrations or demographic changes can provideindications of the species ability to track their suitablehabitats through time. For the pond snail Radix balthica(L., 1758), Cordellier & Pfenninger (2009) explicitlytested this assumption before projecting the speciesfuture potential range. The authors applied a modelselection approach to infer the location of LGM refugia.Subsequently, they used environmental niche modellingand the species current distribution to assess temporalniche shifts. Their data supported climatic niche conser-vatism in R. balthica, allowing them to predict the

potential future range of the species using forecastingSDM. Their analysis suggests that GCC will have animmense detrimental impact on the southern and cen-tral European populations of R. balthica.

How are neutral and non-neutral genetic diversitylinked to adaptive capacity under GCC?

Genetic diversity, phenotypic plasticity and local adaptation. Tol-eration of changing GCC conditions or avoidancethrough habitat shift is dependent on sufficient levels ofadaptive capacity or ecological plasticity in affected spe-cies or populations. There is an inherent link between thestanding genetic variation in a population and theirpotential for adaptation, but this link is not well docu-mented in the GCC literature. Recent studies on trout



(Jensen et al. 2008) and butterflies (Fischer & Karl 2010)illustrate that information about life history traitresponses along an environmental gradient or to chang-ing climate conditions provides insight into the adaptive

capacity of species by illustrating the degree of life his-tory plasticity in a (meta)population’s gene pool. Geneticvariation and adaptive potential across a species’ genepool and adaptation can be important to help tolerate

Grid cells sampled

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Fig. 2 Schematic proceeding to estimate the loss of genetic diversity under global climate change. The species range in this fictionalexample is shaded in grey. Sampling sites are shown as filled circles; the colour indicates the clade found at the respective samplingsite. Grid cells for species distribution models (SDM) modelling are indicated by squares, and grid cells unsuitable in the future areshaded. It is assumed that the sampling sites have been comprehensively sampled. (a–e) Work flow for studies especially designedfor the purpose. (a) Sampling required to achieve comprehensive coverage of desired spatial resolution, (b) test whether sampling atdesired clade level was complete, (c) if necessary, sample the grid cells again, (d) test again for completeness and (e) make projec-tions. (f–i) Work flow for an existing data set. (f) Existing, nonsystematic sampling (g) determine comprehensively sampled cladelevel and associated appropriate sampled number of grid cells for SDM, (h) determine whether effective number of sampled gridcells is actually reached with given resolution, (i) rescale grid if necessary, if repeated rescaling does not provide satisfactory resultsor spatial sampling is imbalanced, sample additional sites and (j) make projections. Figure from Pfenninger et al. (2012).



new conditions but also when selection acts on dispersalcapabilities of species (Canale & Henry 2010). Ultimately,life history traits and resulting phenotypes are the factorsthat determine whether a species or population is able tocope with GCC, not neutral genetic variation (Callaghanet al. 2004). Thus, there is a great need to better under-stand the genomic basis for life history traits, their regu-lation and resulting phenotypes and their respectivevariation.Phenotypic plasticity, that is, an individuals’ capacity

to regulate its physiology to best cope with prevailingor changing environment conditions (Canale & Henry2010) is an important mechanism for dealing with GCC.Details on phenotypic plasticity are poorly known formany groups of organisms, particularly for diversebiota that are difficult to work with experimentally, forexample, many marine species (Hallegraeff 2010). Maxi-mizing an individual’s ability to respond to changingenvironmental conditions comes at the cost of reducingenergy inputs elsewhere, for example, reproduction(Canale & Henry 2010). Thus, there are limits to thepotential phenotypic plasticity of individuals, popula-tions and species. As a direct consequence, phenotypicplasticity should be highest in long-lived organisms asthey cannot withstand high selective pressures, due toslow generation times (Canale & Henry 2010), and needto invest energy in reproduction less frequently thanspecies with short generation times (Pianka 1970). Treesare an exception of long-lived organisms that canrapidly adapt to changing environmental conditionsdue to the immense effective population size, highgenetic variation (even in individual trees) and greatreproductive potential (Petit & Hampe 2006). Canale &Henry (2010) recently reviewed adaptive plasticity invertebrates and conclude many species responses toGCC are linked to plasticity rather than genomic adap-tation. This finding highlights the need for much moremultiple scale ‘omics’ research, not only focussing ongenomics, but also on transcriptomics and proteomicsin our efforts in understanding species’ stress responses(Wullschleger et al. 2009). The results also show thatbesides detailed experimental studies examining ‘omic’responses to GCC, the life history traits of a target spe-cies should be studied or at least evaluated before mak-ing predictions about species potential responses toGCC, although we recognize that this will probablyremain feasible only for a fraction of organismal biodi-versity. Yang et al. (2011) show, for example, that puta-tive specialist species may be less specialized to thefactors they were considered specialists for, but morespecialized for other, previously ignored conditions (e.g. habitat vs. climate niche). Engelhardt et al. (2011) findevidence for a shift in dispersal behaviour of an aquaticinsect. Wing length polymorphism observed in many

other insect taxa has been linked to genetic controls(e.g. Westermann 1993), environmental cues (e.g.Aukema 1990) or a combination of both (e.g. Aukema1990), suggesting that in some species dispersal capacityis highly plastic.Increased efforts to combine basic autecological

research with the study of adaptive and neutral geneticdiversity (e.g. Brown & Paxton 2009; Angeloni et al. 2012)as well as future range projections as advocated byDawson et al. (2011) to assess species vulnerability underGCC conditions will aid assessments of GCC impacts.Environmentally responsive plasticity (polyphenism)that is linked with genetic polymorphism betweenindividuals may also be a first step in the evolutionaryprocess (see Schwander & Leimar 2011 for a recentreview). Thus, preserving (or losing) the varying degreesof plasticity within individual populations of a morpho-species has evolutionary implications as well.

Species with small ranges. Small-range species are consid-ered more strongly threatened by GCC (Hering et al.2009; Morueta-Holme et al. 2010) and provide anotherexample where plasticity is very important to assessGCC impacts. Small-range species with low effectivepopulation size are more likely to have low geneticdiversity and thus reduced adaptation potential, andsmall-range endemics of colder climates (high altitudeor high latitude) may be locally adapted to colder cli-matic conditions. This makes them primary targets forconservation efforts (see Box 2), but the degrees towhich most of these species are really climate sensitiveremains unclear, because little is known about theecological and phenotypic plasticity of most species.

Stress tolerance and gene expression. An increasing num-ber of studies have examined links between intraspecificgenetic variation and stress tolerance. Many studies linkmeasures of neutral genotypic diversity with fitnessparameters. For example, Procaccini et al. (2007) linkedgenotypic diversity with population growth and resil-ience to perturbation in seagrasses. Williams (2001) pre-sented evidence that genetic diversity is linked toincreased sexual reproduction and stronger vegetativepropagation for eelgrass populations exposed to thermalstress. Using microsatellites, Nowak et al. (2009) showthat chemically stressed midge populations significantlydecrease their levels of neutral genetic diversity afteronly 12 generations resulting in a lowered fitness whenexposed to a second stressor (Vogt et al. 2010). It has tobe noted, however, that the theoretical basis underlyingheterozygosity-fitness correlations (HFC; Hansson &Westerberg 2002) is not fully understood and remainsdebated (Szulkin et al. 2010). Models and empiricalevidence indicate that inbreeding will only be reflected



in neutral diversity markers under certain conditionsthat are only met in endangered species with a recentpopulation history involving strong inbreeding (Ballouxet al. 2004; Slate et al. 2004; see also Box 2). More recentevidence, however, seems to support the suitability ofcommonly applied multilocus markers under the assump-tion of a certain degree of inbreeding in the respectivepopulation (Szulkin et al. 2010), but with high levels ofuncertainty. Modern marker systems that allow genome-wide scans of genetic diversity will likely add to theunderstanding of commonly observed HFC and provideimproved accuracy in estimations of inbreeding coeffi-cients (Chapman et al. 2009).More recently, studies have moved towards linking

genetic diversity with responses in gene expression. Bah-rndorff et al. (2010) examined heat shock resistance inisogenic lines of springtails and observed variations inexpression of response genes, although they were unableto detect significant correlations between response geneexpression and thermotolerance. While several studieshave found genetically controlled changes in traits inresponse to stress, a direct link between neutral and non-neutral genetic diversity and concrete stress response israrely found (Hoffmann & Daborn 2007), except of theobservation that in small and genetically impoverishedpopulations inbreeding depression is frequentlyenhanced under stressful environments and may enforcethe extinction risk of populations (Armbruster & Reed2005; Nowak et al. 2007). Measuring neutral genetic vari-ation is still valuable because it is likely to complementadaptive capacity (Scoble & Lowe 2010) and because itreflects important aspects of genetic diversity (populationdynamics and migration, drift, mutation) that are rele-vant for assessing the impact of GCC on genetic diversitypatterns (Sgr#o et al. 2011). It is, however, also clear, thatthere is a necessity to further examine non-neutralgenetic diversity to better assess the adaptive capacity ofpopulations (Kramer & Havens 2009) and gain a bettermechanistic understanding of species responses to GCC.

Where is potential for future research?

Despite the wealth of studies dealing with the GCC onspecies distribution, the number of studies thatincorporate genetic diversity is still quite limited.Above, we argued why GCC impact studies canbecome much more realistic and in many ways morerelevant if they account for or integrate intraspecificgenetic variation and effects on this variation. Here, weoutline approaches and areas of research that webelieve would further our understanding on the issue.To date, most research on genetic impacts of GCC

has focused on neutral genetic variation, either from atheoretical point of view (e.g. Arenas et al. 2012) or in

empirical studies (e.g. Hallatschek et al. 2007; Pfennin-ger et al. 2011; Rubidge et al. 2012). This is mainlyresulting from the ease and low cost of assessing thislevel of genetic diversity in nonmodel organisms. Micro-arrays, quantitative PCR (qPCR) and next-generationsequencing now also allow assessing climatically rele-vant loci (Reusch & Wood 2007). Genome scans usingamplified fragment length polymorphisms (Jump et al.2006, 2008), SNP–based methods or differential display(Miyakawa et al. 2010) allow screening genome-widediversity at both neutral and functional sites even forlarge-scale studies at a reasonable cost and effort(Davey et al. 2011). Such approaches are particularlyeffective for species with a sequenced genome (Hohen-lohe et al. 2010; Tollrian & Leese 2010). Microsatellitesare well established as population genetic markers andare reasonably easy and cheap to develop. Recent stud-ies have shown that microsatellites can also indicateselective loci, for example, through hitchhiking selectionof other candidate loci that can for example be detectedscreening of EST libraries (Nielsen et al. 2009). First pio-neering studies in the GCC framework start to emergeusing this technique on model species like A. thaliana(e.g. Fournier-Level et al. 2011; Hancock et al. 2011), butalso nonmodel species like the butterfly Aricia agestis(Denis & Schifferm€uller, 1775) (Buckley et al. 2012).These kinds of studies will ultimately allow scientists toassess the grade of current local adaptedness of popula-tions to current climate conditions, which genes areresponsible for adaptation to changing environmentalconditions, and the genetic basis for phenotypic plastic-ity responses to GCC.Making the functional link between particular candi-

date genes, their geographical distribution and theirenvironmental relevance remains a complicated endeav-our that is time-consuming, experimentally tricky andcostly. In the foreseeable future, these approaches willprimarily remain suitable only for a few taxa that areexperimentally tractable. Transferability of resultsamong taxa would make single taxon studies more rele-vant, but this remains to be tested. Thus, examiningneutral genetic variation as a simple but rough proxyfor adaptive variation is still relevant, and it is likely toremain so for years to come. However, with the recentlyintroduced poolseq method (Futschik & Schl€otterer2010), population genomic approaches covering theentire genome have the potential to soon becomecommonplace far beyond model organisms (Fabianet al. 2012).The use of putatively neutral genetic variation as a

proxy would be even more valuable, if we had a quanti-tative overview of the link between (neutral) genetic var-iation and quantitative, selectively non-neutral variationand phenotypic or functional variation. The currently



available studies appear to suggest a relatively weakconnection (Reed & Frankham 2001; Leinonen et al.2008; Olano-Marin et al. 2011; Szulkin & David 2011).This relation is likely to vary among taxa due to varia-tion in genome size or intron/exon ratios. A broad taxo-nomic overview, however, is currently still lacking.Similarly, establishing a functional link between theoften shown correlation of (neutral) genetic diversitywith population and individual stress resilience (e.g.Nowak et al. 2007) appears a rewarding issue, not onlyin the GCC debate. One way to integrate most of theabove identified research approaches is the QST/FSTframework (Whitlock 2008; Le Corre & Kremer 2012)that is currently rarely used in a GCC context, but seeFrei et al. (2012) for an exception. However, not all taxacan be bred as required for this type of analysis. If theorganism is at least experimentally tractable under com-mon garden conditions, the PST/FST framework (Brom-mer 2011) may provide an attractive alternative, inparticular in conjunction with SNP-based genome scans(Edelaar et al. 2011). Using such an approach, Nemec et al.(2012) could show that variance in population growth rateas a response to exposure to different temperaturesamong populations of nonbiting midges (Chironomus ripa-rius Meigen 1804) along a climatic gradient is partiallyexplained by variance in genetic diversity. Otherwise,genome scans combined with association mapping (Holli-day et al. 2010; Mariac et al. 2011) can be a feasible way tolink candidate loci and phenotypic variation with environ-mental variation.In current studies on the effects of GCC on genetic

structure, spatial climatic gradients are often used as asurrogate for climate variation over time (Ara!ujo & Rah-bek 2006). However, natural archives preserving DNA(Angeler 2007; Magyari et al. 2011), museum collections(Wandeler et al. 2007; B!alint et al. 2012; Rubidge et al.2012) or monitoring programmes using cryobanking(Lermen et al. 2009) provide valuable and still underusedresources for genetic material from time series and allowdirect study of GCC-related genetic changes in popula-tions and species over time. For other temporal changesof human-induced environmental conditions sucharchives have been successfully used to understandchanges in the hybridization patterns of Daphnia spp.M€uller, 1785 (Brede et al. 2009). Up to now, there are nopublished studies using biological archives to study cli-mate-driven changes in the distribution of genetic diver-sity over time, but as we are aware of some ongoingprojects, these are likely to appear in the near future.Few studies to date have explicitly addressed the

impacts of increased climate variation on the geneticdiversity. The few studies that have, for example Avolioet al. (2012), show that the responses are relatively com-plex and that increased variation can have direct

impacts on the selective regime of species. This can berelated to dispersal, tolerance of extreme temperature ormoisture conditions, or phenotypic plasticity but is notlimited to these aspects. Experimental evolution studies[see Kawecki et al. (2012) for a recent review] hold thepotential to address these aspects if short-term climatevariation is incorporated into the experimental design.We expect that good experimental systems and particu-larly multigeneration studies will provide much insightinto the interaction of climate change, climate variationand genetic diversity.Dawson et al. (2011) propose an integrated approach

to assessing impacts of GCC on biodiversity that inte-grates these aspects and focuses on species vulnerabilityunder GCC conditions based on (i) a species’ sensitivityto climate change conditions, (ii) a species’ adaptivecapacity and (iii) a species’ exposure to changing cli-mate conditions. The authors propose making use ofthe rich palaeontological, ecological and evolutionaryliterature to assess adaptive capacity and sensitivity ofspecies to changing climate conditions and using distri-bution modelling to assess their future exposure. Simi-larly, integrating knowledge from phylogeography andSDM has the potential to assess a species GCC vulnera-bility by addressing aspects on sensitivity (e.g. pastmigration, population structure), adaptive capacity(e.g. estimates of genetic lineages and neutral geneticvariation) and exposure (SDM).As outlined throughout this review, intraspecific

diversity assessments can help inform current and pastdispersal of species and populations and help imple-ment more realistic dispersal scenarios in GCC studies.Hoffmann & Sgro (2011) summarize different GCCresponse models that highlight the importance of demo-graphic factors on the adaptive responses of species.These are often linked to effective population sizes assurrogates for genetic variation and different modes ofgene flow. Improvements on these models and applyingthese models to species with sufficient background dataoffer important research opportunities in GCC biodiver-sity assessments. Simulation studies that use differentmigration scenarios can help us understand the biasesin genetic diversity projections that are implicit inspecies or population projections that account formigration. Jay et al. (2012) introduce an approach calledancestry distribution models to estimate the admixturecoefficients from putatively neutral markers based ontheir correlation with spatial and environmental data.This approach allows making predictions about thefuture displacement of contact zones between popula-tions. Such developments promise great improvementsin forecasting population genetics of species and offerimportant complements to more traditional SDM-basedapproaches. Additional improvements on SDM relate to



the importance of climatic parameters vs. other ecologi-cal parameters for species distributions in general,implementing more realistic migration models andmodels of habitat heterogeneity and fragmentation(Cobben et al. 2011), accounting for life history and eco-logical traits of species (e.g. mode of inheritance, gener-ation, Cobben et al. 2011), choosing the correct scale formodelling (Pfenninger et al. 2012; see also Box 3),assessing the potential of cumulative effects of multiplestressors in GCC projections (Hof et al. 2011a; M€ulleret al. 2012) and integrating species interaction networksto account for potential biotic multipliers of climatechange (Ara!ujo et al. 2011; Zarnetske et al. 2012). Asboth the SDM methodology and our understanding ofnon-neutral genetic responses to environmental condi-tions in general and GCC conditions in particular pro-gress, it may become possible to incorporate localadaptation in GCC models and projections (Atkins &Travis 2010), thus realizing the link of GCC projectionswith assessments of functional genetic diversity andecological genomics. Ultimately, these integrativeapproaches in particular promise to become excitingresearch avenues in climate change biology.

Conclusions

As it is the foundation of biodiversity, inclusion of intra-specific genetic diversity into climate change assessmentsis essential. To date, however, most studies on GCCimpacts, particularly those making predictions aboutfuture species ranges under GCC conditions, are basedon nominal morphospecies and ignore intraspecificgenetic diversity. This is a fundamental shortcoming, asit is clear that the effects of GCC vary among popula-tions. Evidence for this phenomenon comes from manydifferent approaches including direct assessment of cli-mate-adaptive genetic loci in geographical populations(Fournier-Level et al. 2011; Hancock et al. 2011), projec-tions of future population genetic structure of genome-wide genetic diversity (Jay et al. 2012), assessments of cli-mate change responses of populations based on neutralgenetic diversity (Sork et al. 2010; Yang et al. 2011) andassessment of biodiversity losses under GCC conditions(B!alint et al. 2011; Alsos et al. 2012). Including geneticdiversity into GCC studies promises much improvedprojections of species vulnerability and future distribu-tions, particularly in species where detailed informationon the adaptive level of GCC responses is lacking. This iscurrently the majority of nonmodel organisms andclearly highlights the importance of further empiricalstudy to test the evolutionary potential of species, popu-lations and genotypes (Hoffmann & Sgro 2011).Besides potentially improving GCC projections, incor-

porating aspects on intraspecific genetic diversity into

global change biology offers exciting new integratedresearch possibilities, particularly in the advent ofaffordable, widespread use of both neutral and func-tional genetic variation and the increasing availability ofgenomic resources for nonmodel organisms. Ultimately,the processes of GCC response can only be understoodat this level, while studies of neutral genetic variationprovide a framework for identifying species or popula-tion of particular importance and threat under GCC butcannot provide insight on the genetic response mecha-nisms to GCC. Finally, the integration of neutral andfunctional genetic diversity with a better understandingof the autecology of species, for example, from moreexperimental or observational studies, but also fromindirect inferences like the ones outlined in this reviewfrom phylogeography, will provide clearer insights intoshort-term responses to GCC and provide the basis forpredicting the responses of species to ongoing GCC.

Acknowledgements

We thank Sami Domisch, Daniela Eisenacher, Angelica Feur-dean, Christian Hof (all Frankfurt), Florian Leese (Bochum),Klaus Schwenk (Landau), Louis Bernatchez (Laval), MeghanAvolio (New Haven) and two anonymous reviewers for help-ful comments and discussions that helped improve the manu-script. The study was financially supported by the researchfunding programme ‘LOEWE-Landes-Offensive zur Entwick-lung Wissenschaftlich-€okonomischer Exzellenz’ of Hesse’s Min-istry of Higher Education, Research, and the Arts.

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S.U.P. and M.P. planned the review, S.U.P., M.P. andC.N. drafted the manuscript; all authors edited themanuscript and approved the final version.



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