Climate Change and Evolutionary Adaptations at Species' Range Margins

EN56CH08-Hill ARI 14 October 2010 10:51

Climate Change andEvolutionary Adaptationsat Species’ Range MarginsJane K. Hill, Hannah M. Griffiths,and Chris D. ThomasDepartment of Biology, University of York, YO10 5DD, United Kingdom;email: [email protected]

Annu. Rev. Entomol. 2011. 56:143–59

First published online as a Review in Advance onAugust 30, 2010

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-120709-144746

Copyright c© 2011 by Annual Reviews.All rights reserved

0066-4170/11/0107-0143$20.00

Key Words

dispersal, flight morphology, geographic distribution, habitatselection, invasions, postglacial expansion

Abstract

During recent climate warming, many insect species have shifted theirranges to higher latitudes and altitudes. These expansions mirror thosethat occurred after the Last Glacial Maximum when species expandedfrom their ice age refugia. Postglacial range expansions have resulted inclines in genetic diversity across present-day distributions, with a reduc-tion in genetic diversity observed in a wide range of insect taxa as onemoves from the historical distribution core to the current range mar-gin. Evolutionary increases in dispersal at expanding range boundariesare commonly observed in virtually all insects that have been studied,suggesting a positive feedback between range expansion and the evo-lution of traits that accelerate range expansion. The ubiquity of thisphenomenon suggests that it is likely to be an important determinant ofrange changes. A better understanding of the extent and speed of adap-tation will be crucial to the responses of biodiversity and ecosystems toclimate change.

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Ice age refugia:locations to whichspecies retracted toduring glacial periodsand from whichspecies subsequentlyspread during warmer,interglacial periods

Genetic erosion: lossof genetic diversityand reducedheterozygosity withinpopulations

INTRODUCTION

Recent global climate warming has causedspecies to shift their ranges poleward (90, 91).Insects are poikilothermic (cold-blooded) or-ganisms and so are particularly sensitive to tem-perature changes, especially those species thathave narrow thermal tolerances (1, 31). Thereis now a substantial literature documenting thatinsects are expanding at their high-latitude andhigh-elevation cool range margins (2, 58, 90,91, 115) and retracting at their low-latitudeand low-elevation warm margins (2, 37, 88,118). Regardless of any climate change miti-gation that may occur in the future to reducethe release of greenhouse gases, there is a com-mitment to future warming due to continuingemissions from existing industrial and agricul-tural activities, and there are lags in the cli-mate system resulting from thermal inertia inthe oceans. Even the most optimistic scenar-ios mean that there is the inevitability of fu-ture warming for most if not all of this cen-tury (72, 73, 81, 116). Thus, understanding thefactors affecting the pattern and rate of changein species’ ranges is crucial for making reliablepredictions of the potential future distributionof biodiversity as climates continue to warm.

Responding to global climate change is nota new phenomenon for insects. For examplein Britain, the distributions of many butterflyspecies have fluctuated over the past two cen-turies (5), probably related to climate fluctua-tions (65). Many species occupy temperate re-gions because they colonized these regions afterthe last ice age, and evidence from postglacialrange expansions has been proposed as indica-tive of a species’ capacity to respond to cur-rent climate change (6, 24, 34, 35, 70). Speciescan respond to climate change by adapting toclimate changes in situ, by migrating to newclimatically suitable areas and tracking climatechanges, by dying out, or by some combinationof these. For beetles, evidence from the fossilrecord suggests that adaptation of species wasnot observed following postglacial range expan-sion, but that species shifted their ranges totrack the changing climate (23). However, fossil

evidence may not preserve evidence of adapta-tion, and current data indicate that evolution-ary changes in response to current warming arecommonly observed in insects.

During recent climate warming, specieshave been faced with shifting their distributionsacross heavily fragmented, human-modifiedlandscapes and many species are failing to colo-nize new areas and thus failing to track climatechanges (82, 115). For these species, their po-tential for adaptation to new climatic conditionsmay be crucial to their longer-term persistence.Those insects that are tracking climate changesmay also undergo evolutionary changes. The-oretical studies support the notion of increaseddispersal evolving during range expansion (33,68), and increased dispersal ability has been ob-served in species at their expanding range mar-gins. In this paper, we review empirical evidencefor such evolutionary changes occurring ininsects.

Shifts at the leading edge of range expan-sion may often be achieved by small numbersof long-distance migrant individuals, poten-tially resulting in founder bottlenecks. Bottle-necks associated with postglacial range expan-sions have resulted in latitudinal gradients ofgenetic diversity across species’ ranges, from iceage refugia to high-latitude range margins (57).These clines in genetic diversity may affect theability of populations to adapt to future climatewarming. In addition, anthropogenic habitatfragmentation may alter dispersal rates (60) andgene flow among populations, further affect-ing patterns of genetic diversity across species’ranges. Changes to the distributions of speciesin the future are also likely to result in the lossof genetic diversity at low-latitude and low-elevation warm range boundaries where climatewill become unsuitable (i.e., too hot and/or dry).In these locations, which are often the geneti-cally richest parts of species’ ranges, popula-tions are likely to become fragmented, leadingto genetic bottlenecks and genetic erosion asa result of reduced gene flow among isolatedpopulations (57). However, survival of popula-tions at the trailing edges of species shifting dis-tributions can be particularly important to the

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Range shifts:expansion poleward atspecies’ leading-edge,cold, high-latituderange boundaries andretractions poleward attrailing-edge, warm,low-latitude rangeboundaries

Leptokurtic dispersalpattern: thedistribution ofdispersal distancestraveled by a sample ofindividuals can beplotted on a graph as adispersal curve orkernel

persistence and evolution of species (47). Thus,examining patterns of genetic diversity acrossinsect ranges, and considering how these pat-terns might affect species’ potential to evolveand adapt to climate changes, is important forbiodiversity conservation.

SCOPE OF REVIEW

In this review, we consider the impacts of cli-mate warming on insect distributions, and wefocus on examining evolutionary changes at themargins of species ranges. The review coversthree main aspects: (a) We describe currentgeographical patterns of genetic diversity andevolutionary adaptations at range margins aris-ing from postglacial range shifts. (b) We reviewevolutionary adaptations at recently expandingrange margins. (c) We discuss the implicationsof these adaptations for species’ abilities to re-spond to future climate warming, and highlightcurrent knowledge gaps.

Geographical Patternsin Genetic Diversity

Evidence from plant and animal fossil remainssuggests that at the height of the Last GlacialMaximum (LGM; around 25,000 years ago; 22)many members of Northern Hemisphere ter-restrial biota had distribution ranges that weresignificantly smaller, as well as farther south,than those observed today (56). The climate be-gan warming after the LGM, then cooled againduring the Younger Dryas period, followed bywarming around 12,000 years ago (104) as cli-matic conditions shifted rapidly toward the cur-rent, full interglacial (Holocene), warm con-ditions. Many species rapidly expanded theirrange boundaries northward out of these south-ern refugia, tracking the retreating ice sheetsand favorable climatic conditions (56).

In species with long-distance leptokurtic(i.e., with a long “tail”) dispersal patterns, colo-nization of new habitats may come about froma small number of founder individuals dispers-ing over long distances, which may lead to aloss of alleles and reduced heterozygosity in

these newly colonized sites (55, 56, 71, 97,106). By contrast, species with a lower incidenceof long-distance dispersal tend not to showsuch marked clines in genetic diversity; in thesespecies, many individuals repeatedly colonizesites over relatively short distances, such thatthere is greater gene flow and mixing of allelesamong subpopulations (55, 71). Nonetheless,a commonly observed consequence of rapidpostglacial expansions is the genetic impover-ishment of populations inhabiting newly colo-nized areas compared to those residing in areasof persistently suitable habitat (55). This hasbeen demonstrated in a wide variety of insecttaxa, including Lepidoptera, phasmids, weevils,pitcher-plant mosquitoes, grasshoppers, caddisflies, bees, Megaloptera, and cicadas (3, 4, 11,17, 30, 45, 54, 55, 79, 83, 94, 117). The patternsare indicative of rapid postglacial range expan-sion in many regions of the globe includingEurope (11), North America (36), New Zealand(16, 79), and Asia (3). However, in some stud-ies these latitudinal cline effects are relativelyminor (98) or not evident at all (75, 99, 112).Variation among species is likely to reflect dif-ferent patterns of dispersal and habitat availabil-ity, coupled with differences in life-history traits(e.g., affecting population growth) and differentnumbers and locations of refugial populations.In the tropics and subtropics, variation in mois-ture availability is likely to have been as impor-tant as temperature in determining fluctuationsin insect distributions in response to glacial andinterglacial climates. In Australia, the caddis-fly Tasimia palpata appears to have expandedduring interglacial periods, associated with theexpansion of subtropical rainforests (85); dungbeetle phylogeographies and speciation also re-flect the historical dynamics of rainforests (8).

The loss of within-population variation as-sociated with range expansion is sometimes,but not always, accompanied by losses of large-scale among-population variation. For exam-ple, populations with different refugial popu-lations from the Iberian, Italian, and Balkanpeninsulas of Europe (as well as farther east,within Asia) are often regarded as separate racesor subspecies (77, 111). In many species, not

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Quaternary: thegeological periodencompassing the past2.6 million years

all of these refugia contributed to the north-ward spread that took place under warmerHolocene conditions, such that northern pop-ulations commonly represent only a subset ofthe southern refugial lineages (57, 77, 114).

Some studies have shown that spatial pat-terns of genetic diversity reflect the existenceof more ancient refugia that predate the lastglacial period (78). This is particularly the casefor species that are adapted to cool environ-ments and would, in many cases, have beenmore widespread during glacial climates; theircurrent distributions may represent Holocene(interglacial) refugia. For example, the cold-adapted European leaf beetle Gonioctena pal-lida has a hotspot of genetic diversity inthe Carpathian Mountains in central Europe,which implies that current patterns of geneticvariation in this species reflect a Pleistocene cli-matic event that resulted in population isolation>90,000 years ago, well before the end of thelast ice age (78). Other studies demonstrate ev-idence of repeated glacial/interglacial cycles oncurrent patterns of genetic diversity, with likelyrange expansion during glacial periods (25).

Closer focus on butterflies. One well-studied taxon in terms of phylogeography andregional patterns in genetic diversity is but-terflies. Genetic differentiation among threestrongly divergent lineages of the satyrid but-terfly Maniola jurtina across Europe demon-strates the genetic consequences of past iso-lation of populations associated with differentglacial refugia (44). Similar genetic patterns,showing distinct lineages within currently con-tinuously distributed populations, have alsobeen observed in several other butterfly species(11, 46, 100, 102). Studies of Coenonympha ar-cania (11) that compared the genetic structureof populations across the species’ Europeanrange have demonstrated a latitudinal cline inallele frequencies from south to north (56, 71).Isolated peripheral populations at northernrange boundaries displayed significantly lowerlevels of genetic variation and high differentia-tion, while central and southern populations (inareas of previous glacial refugia) showed much

higher genetic diversity and no significant dif-ferentiation. These findings correspond to a re-duction in polymorphic loci from 64% in pop-ulations of C. arcania in southeastern Europe to27% in populations at the northern periphery ofits range in Sweden (11). By contrast, no south-north decline in genetic diversity was observedin Europe for two sibling species of butterfly,the marbled white Melanargia galathea and theIberian marbled white M. lachesis (46), and highgenetic diversity in M. galathea has been pro-posed as one reason for its recent range expan-sion at its northern range limits (46). However,genetic differentiation is commonly high be-tween different population refugias, comparedto areas of postglacial expansion. This is becauseonly a subset of refugial populations may giverise to the new range, and this will be combinedwith the loss of variation associated with rangeexpansion itself (57).

Comparison of three species of satyrid but-terfly in Britain (61) showed that these speciesdiffered in their genetic diversity. The specieswith more extensive current ranges in Britainhad greater genetic diversity (Maniola jurtina >

Pyronia tithonus > Pararge aegeria). Greater ge-netic diversity may reflect longer occupancy ofthese regions by species since the LGM, greaterhabitat availability, and therefore more geneflow, or it may reflect more recent fluctuationsin ranges over the past two centuries (63). A ge-netic study of the host-specific butterfly Parnas-sius smintheus (Papilionidae) and its larval hostplant Sedum lanceolatum (Crassulaceae) showedthat the two species responded to postglacialclimate warming in similar ways (through re-peated uphill contractions and downhill retrac-tions during climate fluctuations) but indepen-dently (patterns of within-population geneticvariation and among-population differentiationshowed no congruence) (26).

Implications for population persistence inthe future. Evidence from a wide range ofinsect groups leads us to conclude that dif-ferences in dispersal potential, along withthe climatic events of the past two millionyears (the Quaternary period), have had major


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Anthropogenicclimate change:refers to recent climatewarming attributableto human activities andinfluences ongreenhouse gasemissions

influences on the current patterns of genetic di-versity evident within the distributions of manyinsects (56). Reduction in genetic diversity asa consequence of postglacial expansion meansthat, for many species, the lowest genetic di-versity is found in populations that inhabit re-gions at the cool, leading margins of species’ranges. Hence, recent climate-driven range ex-pansions will involve individuals from popula-tions at range boundaries that already exhibitreduced allelic diversity arising from postglacialrange expansions.

However, there is relatively limited knowl-edge of when these genetic effects mightaccelerate or limit distribution changes, rel-ative to that expected in the absence of suchgenetic effects. Genetic bottlenecks representa double-edged sword during range expansion.On the one hand, they may result in the reducedcapacity for subsequent adaptation and poten-tially in the fixation of deleterious alleles; on theother hand, they may result in the rapid fixationof traits that facilitate fast range expansion andhence survival during a period of rapid climatechange. However, loss of genetic diversity hasbeen associated with reduced fitness leading topopulation declines in some insects (101). InPolyommatus coridon (Lycaenidae), populationswith lower genetic diversity have reducedadult lifetime expectancy, reduced dispersal,and smaller population size (113). Given thatprevious studies have demonstrated a linkbetween lower genetic diversity and increasedlocal extinction of populations (96), the impactof current range expansion and populationbottlenecks as species spread through human-dominated landscapes could be expected toresult in reduced fitness, and this could reducethe rate of expansion. In contrast, althoughthe recent range expansion of Battus philenor(Papilionidae) into California has resulted inpopulations with reduced genetic diversity,this has been associated with shifts onto anovel host plant, laying significantly larger eggclutches and loss of mimics in these Californiapopulations. This implies that losses in geneticvariation may be compensated by increases inadaptation to conditions in the areas that are

being invaded (36). Loss of genetic variationassociated with recent range expansions isexpected to continue in modern landscapesand may be even greater than in the past,given the fragmented nature of many modernlandscapes. As with B. philenor (36), geneticlosses are frequently associated with speciesspreading across landscapes that containpatchily distributed habitats, for example, ingall wasps associated with patches of plantedhost plants (107).

Further range changes associated with cli-mate warming are expected to result in erosionof genetic variation within species (30, 108).Expansions at high-latitude boundaries will beinitiated from populations that already con-tain relatively low levels of variation, and fur-ther founder effects will reduce this even more.Meanwhile extinctions of populations at theirhot, lower-latitude trailing boundaries are ex-pected (64, 103) and observed (90, 118) as aresult of climate warming. These local extinc-tions occur within parts of species’ distributionsthat fall within their historical refugial distri-butions, where within-population genetic vari-ability is greatest. For example, the butterflyCoenonympha arcania shows high genetic diver-sity in parts of its distribution (11) that are pro-jected to become extinct in response to futureclimate warming (103). Hence, within-speciesgenetic variation may be eroded even when thespecies as a whole is not threatened by climatechange. It is unknown whether such genetic at-trition will affect the expected persistence timesand speciation capacities of species that havebeen so-affected.

Evolutionary Adaptations atExpanding Range Boundaries

There is now a considerable body of evidencedocumenting the degree to which animalspecies are responding to recent anthro-pogenic climate change and shifting theirdistributions to high latitudes (89, 91). Thisbody of evidence covers many insect species,but most analysis of climate-driven rangeexpansion has focused on a few well-studied


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groups such as butterflies (90, 93, 115) andOdonata (59), for which there are long-term,fine-scale spatial and temporal datasets record-ing species’ distributions and abundances.Insects colonizing newly available habitats arenot a random subset of the original populationand usually share a suite of life-history traitsassociated with increased colonization ability.In wing-dimorphic species, these effects areevident in terms of increased proportions ofstrong-flying macropterous individuals withinnewly colonized populations (86, 105, 109). Inwing-monomorphic species, such as butterflies,these effects are evident as more subtle changesin adult flight morphology (62) and flightmetabolic rates (43) in newly colonized sites.Many additional traits, such as habitat or hostselection or reproductive strategy, may comeunder selection during range shifts and therebyalso influence the rate of range expansion. Inthis section, we review the types of adaptationsevident at expanding range boundaries anddiscuss how these changes might affect species’abilities to respond to climate change. Weinclude discussion of evolutionary adaptationsarising from climate-driven range expansionsas well as changes occurring through rangeexpansion attributable to other nonclimaticfactors.

Our review focuses primarily on expand-ing range boundaries that involve expansion tohigher latitudes. Although uphill range shiftsare recorded in insects (21, 119), we do notconsider uphill expansions in this review, andin any case these may provide little oppor-tunity for evolutionary adaptation given thatcolonization distances are much shorter, re-sulting in greater gene flow between core andmargin sites. We also do not consider evolu-tionary changes at contracting boundaries forwhich empirical studies are lacking in insects,although there is some such evidence for othertaxa (e.g., beech trees; 74). Evolutionary shiftsin photoperiod sensitivity, and hence phenolo-gies, have taken place throughout the distribu-tion of the pitcher plant mosquito, Wyeomyiasmithii, in the eastern United States since 1972,but responses have been strongest at higher

latitudes, with limited responses at the south-ern boundary (13). Museum specimens of thestream-dwelling beetle Gyretes sinuatus showedan 8% increase in body size and a 6% increasein the length/width ratio of the body over a60-year period in the southern United States.These changes were attributed to cooling lo-cal temperatures over the same period (7), andthis is a possible explanation for the lack ofphenology evolution in southern populations ofW. smithii. There is little or no evidence of theevolution of increased tolerances of high tem-peratures under climate warming (14).

Predictions for evolutionary changes thatmight occur at contracting range boundariesmay mirror changes observed in populationsthat are declining (regardless of where pop-ulations are located within their geographicalrange) and becoming increasingly fragmented.For example, studies of museum specimens ofthe garden tiger moth, Arctia caja, which hasdeclined in abundance by 85% in Britain overthe past 30 years, have provided evidence of asignificant decline in genetic diversity and ofchanges in wing morphology during the twenti-eth century (2). The changes in wing morphol-ogy imply evolution of increased dispersal abil-ity over time, which may be due to evolutionaryresponses to increased habitat fragmentation(2, 10, 68), although nongenetic effects due toenvironmental factors may also be responsiblefor these changes. By contrast, with more ex-treme levels of habitat fragmentation, evolutionof reduced dispersal might be expected in iso-lated island-like populations, as typified by trueoceanic island endemic species (19, 68). Anal-ysis of the morphology of museum specimensshowed likely reduction in flight capacity of theswallowtail butterfly, Papilio machaon britanni-cus, as populations contracted over time (27),but as with all studies of wild-caught material itis difficult to disentangle genetic changes fromphenotypic responses to environmental factors.Common-environment rearing of the Glanvillefritillary butterfly, Melitaea cinxia, showed re-duced dispersal in long-established populations(48). Studies at contracting range boundariesare required to determine the relative effects of


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population size, genetic diversity, and habitatavailability on evolutionary changes.

Morphological changes during climate-driven range expansion. Evidence of evolu-tionary changes in insect populations comesfrom two types of study: long-term tempo-ral studies at specific locations and snapshotcomparisons of populations from different loca-tions. Longitudinal temporal studies examiningmorphological changes over time come fromstudies of museum specimens (7, 27). However,such data are rarely available for recently col-onized populations that have existed only for afew years or decades.

Snapshot studies of evolutionary changesduring range expansion have compared popu-lations at different times-since-colonization bycomparing populations at increasing distancesfrom the expanding range margin. Thesestudies have examined evolutionary changesin adult flight morphology, as well as changesin larval diet. Climate-driven range expansionhas been associated with the exploitation ofa wider range of host plants in some species.The comma butterfly, Polygonia c-album, hasexpanded its northern range margin northwardin Britain by ∼200 km in the past 60 years.This range expansion has been associated withan apparent change in its preferred larval hostplant from Humulus lupulus (hop) to includeother plant species, especially Urtica dioica (net-tle) and Ulmus glabra (wych elm), host plantsutilized in other parts of its European range andby other closely related Polygonia species (15).These new larval host plants are more widelyavailable in Britain compared with H. lupulus,and so changes in larval diet may have facilitatedthe recent range expansion this species has dis-played, especially because butterfly growth andsurvival were higher and adults were larger onthe new plant hosts (15). A similar pattern hasbeen observed in expanding populations of thebrown argus butterfly, Aricia (Plebeius) agestis,where climate warming has been associatedwith a shift in host plant selection by oviposit-ing females from exploiting common rockrose,Helianthemum nummularium, on chalk and

limestone grassland habitats to exploitingErodium cicutarium and Geranium molle incooler microclimates in a wider range of grass-lands (5, 109). As with P. c-album, the potentialto utilize more widely available host plants thatgrow on a variety of geological substrates hasincreased the potential breeding habitats avail-able to A. agestis and thus increased its abilityto expand its range in Britain as the climatewarms. These within-species shifts mirrorbetween-species differences that have been ob-served, in which habitat generalists and speciesthat utilize widespread host plants and habitatsare expanding their ranges faster than thosewith more specialized requirements (115).

Theoretical studies predict that dispersalrates will often evolve at expanding rangeboundaries, and there is considerable empiricalevidence to support this notion. In many cases,this empirical evidence is based on indirectmeasures of insect dispersal based on adultflight morphology. Measures of thorax sizeand shape (which measure flight muscle mass),measures of wing size and shape (aspect ratio;wingspan2/area), and measures of wingloading(insect mass/wing area) are associated withinsect flight speed and maneuverability (9, 20).Differences in morphological traits associatedwith flight and reproduction have been shownin the speckled wood butterfly, Pararge aegeria(62). More recently colonized sites generallyhave populations with larger adults, greaterthorax mass, and broader thorax shape (62, 68,69). Differences in wing aspect ratio are alsoevident, although patterns are not consistent,and both higher (=narrower wings; 68) andlower (=broader wings; 62) aspect ratios havebeen recorded at range margin sites. Thereis also evidence that selection pressures mayvary between sexes, with evolutionary changesmore evident in females than in males duringresponses to climate change (68) and habitatfragmentation (48). Given that butterfliesuse flight for activities other than dispersal,for example, mate location, nectaring, andoviposition, it is perhaps not surprising thatevolutionary adaptations to range expansion donot always predominate over other selection


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pressures. Hence, evolutionary changes inflight morphology are not always evident in re-cently colonized butterfly populations (48, 84).The studies cited above for P. aegeria are fromstudies of F1 offspring reared under commonenvironmental conditions (62, 68, 69), consis-tent with a genetic basis for the change. Studieswhere differences in dispersal morphologyamong populations are evident only in wild-caught material and not in F1 offspring implythat environmental factors at range marginsites, rather than any genetic changes, are af-fecting dispersal morphology, perhaps througheffects of larval host plant quality and/ortemperature on insect development (15, 92).

In studies where changes in flight morphol-ogy are not evident in newly colonized sites,individuals nonetheless have higher dispersalability compared with older populations. Inexpanding populations of the map butterfly,Araschnia levana, butterflies in newly colonizedsites have higher levels of PGi alleles (84),which have been associated with superior flightmetabolic rates and population growth rates(43, 51), even though colonizing individualsshow no changes in wing or thorax measures(84). Similarly, Glanville fritillary butterflies,Melitaea cinxia, have greater dispersal ability innewly colonized sites but show no change intheir flight morphology (48). Empirical mea-sures of dispersal from mark-release-recapturefield studies, as well as physiological measuresof the ADP/ATP ratio in butterfly flight mus-cles (49), provide further support that increaseddispersal capability is present in newly colo-nized populations of M. cinxia in the absenceof any changes in adult flight morphology.

Increased dispersal ability has also beendemonstrated in range margin populations ofother insect taxa (105, 109). A comparison ofthree British damselfly species currently ex-panding their distributions northward showedthat Calopteryx splendens, the most rapidly ex-panding of the three species, had higher wingaspect ratios (=narrower wings) in individ-uals from the range margin compared withthose closer to the core of the range (52).In Orthoptera, the frequency of dispersive

(long-winged macropterous) morphs was ap-proximately eight and four times greater forConocephalus discolor and Metrioptera roeselii, re-spectively, at expanding range margins than inthe core of their ranges (105). Once established,populations of these bush crickets returned tolow levels of macroptery within 5 to 10 years(generations) after colonization. This findinghighlights that evolutionary adaptations can berapid; for example, photoperiodic adaptation inpitcher plant mosquitoes, W. smithii, was evi-dent after 5 years (13).

In many studies, trade-offs between flightand reproduction have been evident (120), andthese trade-offs are particularly strong in taxathat disperse by flight but are capable of com-pleting other adult activities by different means.Captive-reared macropterous females of C. dis-color showed a threefold reduction in fecundity,relative to brachypterous individuals, and thistrade-off is likely to have driven the decline inmacroptery in populations once they had es-tablished. The trade-off is more complex in in-sects that use flight for a variety of purposes.Nonetheless, in the speckled wood butterfly,P. aegeria, the increased dispersal ability of indi-viduals at range margin sites was associated withreduced reproductive investment; range mar-gin females have relatively larger and broaderthoraxes but produced significantly fewer eggscompared with those from core sites (69). Thissuggests that any benefits to species expandingtheir ranges in response to climate warmingfrom evolutionary increase in dispersal abilityare balanced by reduced fecundity and lowerpopulation growth rates in margin sites. Pop-ulations developing under cooler conditionsin range margin sites also show different de-velopment rates (53) and multivoltine speciesdevelop through fewer generations (40), fur-ther contributing to reduced population growthrates at range margin sites. Thus, the bene-fits to expanding species of increased dispersalat range margins may be relatively short-livedbut essential in enabling species to shift theirdistributions.

Evolutionary changes during latitudinalrange expansions have hardly begun to be


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explored for other traits that could be impor-tant for insect population persistence. Follow-ing Quaternary range expansion, many speciesdeveloped genetically based latitudinal clines inphotoperiod and temperature responses (12, 80,87), and in body size and melanism (28, 29, 76,121), within the last ∼10,000 years. As expand-ing populations again spread poleward in re-sponse to anthropogenic climate warming, theselection pressures that generated these clineswill presumably be renewed, but such data arecurrently lacking.

Morphological changes during invasionsand metapopulation dynamics. The studiesdiscussed above are for species expanding theirranges primarily in response to climate warm-ing. However, range expansions of insects col-onizing and invading new areas commonly oc-cur in the absence of climate warming. Thereis a large literature on invasive species showingevolutionary adaptations during range expan-sion, and evolutionary changes are also evidentas a consequence of colonization-extinctionmetapopulation dynamics in fragmented land-scapes. For example, studies of M. cinxia (50)showed altered life-history traits in newly col-onized sites within metapopulations. A meta-analysis of the Mediterranean fruit fly, Ceratitiscapitata (a globally successful invader), showedthat life-history traits such as longevity and fe-cundity differed in newly colonized sites (32).

By contrast to climate-driven range expan-sions, many invasive species that are expand-ing their ranges are not necessarily limited bysuitable climate conditions and so may not ex-perience the same environmental challengesand selection pressures as species expandingin response to climate warming. Nonetheless,the invasive hemlock woolly adelgid, Adelgestsugae, has expanded its range northward in ar-eas with cooler climates, and this has been as-sociated with the evolution of greater cold har-diness (18). Local climate conditions may alsohave resulted in changes in voltinism duringthe invasion of Japan by the North Americanmoth Hyphantria cunea (39). A temperature-related latitudinal gradient in body size evolved

in Drosophila subobscura within two decades ofits introduction to North America (67).

These studies suggest that many of the evo-lutionary adaptations of species expanding theirranges owing to climate warming may mirrorevolutionary responses in expanding species re-gardless of the drivers of range changes. How-ever, for other traits and evolutionary changes,the colonization of newly available climati-cally suitable habitats may result in selectionpressures and environmental challenges differ-ent from other types of range changes. Thismay mean that the traits under selection, thestrength of selection pressures, and the typesof evolutionary adaptation that are evident maynot be comparable between climate-driven andnonclimate-driven range changes.

Implications of EvolutionaryAdaptations

Climate change and the resulting communityand distribution changes of species mean thatvirtually all populations of all species will haveexperienced changes in selection pressures asa result of recent climate change, and this willcontinue for the foreseeable future. The evolu-tionary shifts driven by these changes affect theecology of species and communities, potentiallyresulting in the emergence of new pest speciesand the extinction of other taxa, as flexible, mo-bile generalist species and phenotypes come todominate biological communities (109, 115).Whereas the ecological shifts generated by cli-mate change are increasingly well documented(73, 89, 95), the evolutionary responses are farless well understood, as are the feedbacks be-tween the evolutionary and ecological changesthat are presumably affecting most populationsof species in the world.

Knowledge gaps and future research. Re-cent anthropogenic climate change provides anopportunity to evaluate the role of evolutionin ecology, and vice versa, and the role of evo-lution in permitting species to survive or goextinct. In particular, the feedbacks betweenecology and evolution might be expected tobe strongest at range boundaries, where the


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strength of selection may be greatest and pop-ulation bottlenecks common. The extent andspeed of adaptation could be crucial to theresponses of biodiversity and ecosystems toclimate change, and several areas of researchrequire further attention.

There is no information about whether therate of environmental change might affect thelikelihood and speed of evolutionary responsesat contracting and expanding range margins. Atrange boundaries where conditions are deterio-rating (i.e., trailing edge margins), novel adap-tations will presumably be rare (increasinglylimited by low mutation rates) because most ofthese marginal populations are likely to havebeen under historical directional selection tosurvive in hot/dry conditions in the recent past;the failure to adapt sufficiently rapidly undersuch conditions is likely to result in populationdecline and extinction if conditions becomemore extreme (41, 42). The degree to whichpopulations may or may not adapt to new en-vironmental conditions has not been examinedat the trailing edges of insect species’ distri-butions. Thus, new empirical and theoreticalwork is needed. Laboratory selection experi-ments often show the capacity of populations toadapt to new conditions, but it is unclear howsuch findings might translate to field conditionswhere trailing-edge populations have experi-enced past directional selection and where theymust compete and interact with newly arrivingthermophilous species that may already bebetter adapted to the new physical conditions.Given that evolutionary feedbacks are expectedto reduce rates of population decline whenenvironmental conditions are deteriorating(41, 42), reduced rates of climate changepresumably increase the likelihood of sufficientevolution taking place to enable populations topersist; but this has not been empirically tested.

At expanding range margins, rapid climatechange may increase the likelihood of theevolution of increased dispersal capacity be-cause species lagging behind climate changeswill experience strong directional selection,generation after generation, whereas thosethat are keeping track of climate changes will

experience periodic setbacks in cooler years.Our review has highlighted that the evolutionof dispersal is commonly observed in expandinginsect species. Many studies have highlightedthat the dispersal ability of insects is crucial forenabling them to respond to environmentalchanges (60, 115). Some measures of dispersal,such as distance traveled and incidence of flight,are relatively well understood (through mark-release-recapture studies), as is the evolution ofdispersal (through theoretical simulation mod-els and some empirical examples). However,evolutionary changes to the behavioral andphysiological processes involved in flight in thecontext of climate change and range shifts areless well known. One option for conservationmanagement to help species respond to climatechanges is to develop landscapes that havebetter habitat connectivity and thus aid species’dispersal and tracking of climate, but thepotential success of such a strategy is largelyunknown (66). A better understanding of thebehavioral inclination of individuals to disperse,their behavior at habitat boundaries, and theirlikelihood of traveling across unsuitable habi-tats is required. Investigation into behavioraladaptations of colonizing individuals and newlyestablished populations compared with ances-tral populations and individuals in the core ofthe range may help in developing more resilientlandscapes that better conserve biodiversity.

In general, far less information is availableon the evolutionary responses of populationsin regions where conditions are deterioratingfor those species, at least in insects, comparedwith evolutionary responses at expanding rangemargins (38). Such information is important be-cause evolution in refugial populations may benecessary if species are to survive in the longterm and then recolonize areas at lower lati-tudes, assuming cooler climates occur again atsome point in the future. If populations lackthe capacity to adapt, then projections of futurerange retreats and extinctions are more likelyto be realized (110).

Relationships between species’ genetic vari-ability and their patterns of range expansionare not well understood. For example, it is not


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clear whether species showing the most rapidrange expansions during recent climate changeare those that have high genetic variation be-cause of their high evolutionary capacity. Al-ternatively, species with attributes that facilitaterapid expansion may have lost genetic variationin the past (during rapid postglacial expansions)but are capable of responding rapidly to recentclimate change. More information on the habi-tat associations and life-history traits of speciesthat exhibit reductions in genetic variability asspecies shift their ranges would help in under-standing which species may or may not showadaptations to climate change in the future.

In this review, we have focused on evolu-tionary adaptations along latitudinal gradients,and studies examining evolutionary responsesalong elevation gradients are lacking. Thedistances insects need to move to track climatechange along elevation gradients are far shorterthan those required to track climate with lat-itude (89). Thus, greater gene flow mightprevent local adaptation at low-elevation range

boundaries because of gene swamping fromhigher altitude populations but accelerate therate of evolution at high-elevation boundariesthrough the immigration of warm-adaptedgenes from lower altitude populations. In asimilar manner, it is unknown whether thepatterns that have been observed in specieswith large continental-scale distributions arerepeated in more narrowly distributed species,but at a smaller scale. Again, it is possiblethat increased capacity for gene flow betweenthe leading and trailing range boundariesof narrowly distributed species results inpatterns different from those discussed in thisreview. In the field of evolutionary adaptationsto recent climate change, there are still farmore unknowns than established generalities.Notwithstanding the serious negative impactsof recent climate change on biodiversity andecosystems, we do currently have opportunitiesto examine and understand the feedbacksbetween ecological and evolutionary processesduring a period of rapid environmental change.

SUMMARY POINTS

1. Many species are responding to recent climate change and shifting their distributionsto higher latitudes and higher altitudes. Evolutionary adaptations have been observed atspecies’ expanding high-latitude range margins.

2. Recent range changes mirror those observed during climate warming after the LGMabout 25,000 years ago. These postglacial expansions have resulted in latitudinal declinesin genetic diversity from low to higher latitudes in many species from a wide range ofinsect taxa.

3. Declines in genetic diversity arise when colonization of new habitats is by a small numberof founder individuals dispersing over long distances, which leads to loss of alleles andreduced heterozygosity.

4. It is unclear whether these postglacial genetic effects might accelerate or limit currentrange changes, but loss of genetic variation is likely to continue as species spread acrossmodern landscapes with habitats that are heavily fragmented.

5. Evolutionary changes occur in populations at expanding range boundaries. The mostcommonly observed adaptation is increased dispersal, e.g., changes in flight morphology(wing and thorax), and increased metabolic rates. Changes in habitat associations are alsoobserved.

6. Trade-offs between flight and reproduction are commonly observed such that rangemargin sites have individuals with reduced fecundity.


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7. A better understanding of the extent and speed of adaptation is crucial to the responsesof biodiversity and ecosystems to climate change.

FUTURE ISSUES

1. How does the rate of environmental change affect the likelihood and speed of evolutionaryresponses in expanding species?

2. What is the likelihood of expanding species adapting to new environmental conditions?

3. What are the relative roles of changes in (a) physiological processes underlying disper-sal ability and (b) the behavioral inclination of individuals to disperse in determiningcolonization rates?

4. Are evolutionary adaptations evident at contracting range boundaries, and under whatcircumstances are they fast enough to prevent population extinction?

5. Are evolutionary adaptations observed on latitudinal gradients also evident along eleva-tional gradients, and in species with small geographical ranges?

6. What is the relationship between the genetic diversity of species and their rate of rangeexpansion?

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

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EN56-Frontmatter ARI 28 October 2010 7:29

Annual Review ofEntomology

Volume 56, 2011Contents

Bemisia tabaci: A Statement of Species StatusPaul J. De Barro, Shu-Sheng Liu, Laura M. Boykin, and Adam B. Dinsdale � � � � � � � � � � � � � 1

Insect Seminal Fluid Proteins: Identification and FunctionFrank W. Avila, Laura K. Sirot, Brooke A. LaFlamme, C. Dustin Rubinstein,

and Mariana F. Wolfner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �21

Using Geographic Information Systems and Decision Support Systemsfor the Prediction, Prevention, and Control of Vector-Borne DiseasesLars Eisen and Rebecca J. Eisen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �41

Salivary Gland Hypertrophy Viruses: A Novel Group of InsectPathogenic VirusesVerena-Ulrike Lietze, Adly M.M. Abd-Alla, Marc J.B. Vreysen,

Christopher J. Geden, and Drion G. Boucias � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �63

Insect-Resistant Genetically Modified Rice in China: From Researchto CommercializationMao Chen, Anthony Shelton, and Gong-yin Ye � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �81

Energetics of Insect DiapauseDaniel A. Hahn and David L. Denlinger � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 103

Arthropods of Medicoveterinary Importance in ZoosPeter H. Adler, Holly C. Tuten, and Mark P. Nelder � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Climate Change and Evolutionary Adaptations at Species’Range MarginsJane K. Hill, Hannah M. Griffiths, and Chris D. Thomas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 143

Ecological Role of Volatiles Produced by Plants in Responseto Damage by Herbivorous InsectsJ. Daniel Hare � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 161

Native and Exotic Pests of Eucalyptus: A Worldwide PerspectiveTimothy D. Paine, Martin J. Steinbauer, and Simon A. Lawson � � � � � � � � � � � � � � � � � � � � � � � � 181

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EN56-Frontmatter ARI 28 October 2010 7:29

Urticating Hairs in Arthropods: Their Nature and Medical SignificanceAndrea Battisti, Goran Holm, Bengt Fagrell, and Stig Larsson � � � � � � � � � � � � � � � � � � � � � � � � � � 203

The Alfalfa Leafcutting Bee, Megachile rotundata: The World’s MostIntensively Managed Solitary BeeTheresa L. Pitts-Singer and James H. Cane � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 221

Vision and Visual Navigation in Nocturnal InsectsEric Warrant and Marie Dacke � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 239

The Role of Phytopathogenicity in Bark Beetle–Fungal Symbioses:A Challenge to the Classic ParadigmDiana L. Six and Michael J. Wingfield � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 255

Robert F. Denno (1945–2008): Insect Ecologist ExtraordinaireMicky D. Eubanks, Michael J. Raupp, and Deborah L. Finke � � � � � � � � � � � � � � � � � � � � � � � � � � � 273

The Role of Resources and Risks in Regulating Wild Bee PopulationsT’ai H. Roulston and Karen Goodell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 293

Venom Proteins from Endoparasitoid Wasps and Their Rolein Host-Parasite InteractionsSassan Asgari and David B. Rivers � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 313

Recent Insights from Radar Studies of Insect FlightJason W. Chapman, V. Alistair Drake, and Don R. Reynolds � � � � � � � � � � � � � � � � � � � � � � � � � � � 337

Arthropod-Borne Diseases Associated with Political and Social DisorderPhilippe Brouqui � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 357

Ecology and Management of the Soybean Aphid in North AmericaDavid W. Ragsdale, Douglas A. Landis, Jacques Brodeur, George E. Heimpel,

and Nicolas Desneux � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

A Roadmap for Bridging Basic and Applied Researchin Forensic EntomologyJ.K. Tomberlin, R. Mohr, M.E. Benbow, A.M. Tarone, and S. VanLaerhoven � � � � � � � � 401

Visual Cognition in Social InsectsAurore Avargues-Weber, Nina Deisig, and Martin Giurfa � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 423

Evolution of Sexual Dimorphism in the LepidopteraCerisse E. Allen, Bas J. Zwaan, and Paul M. Brakefield � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 445

Forest Habitat Conservation in Africa Using Commercially ImportantInsectsSuresh Kumar Raina, Esther Kioko, Ole Zethner, and Susie Wren � � � � � � � � � � � � � � � � � � � � � � 465

Systematics and Evolution of Heteroptera: 25 Years of ProgressChristiane Weirauch and Randall T. Schuh � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 487

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Documents

Climate Change and Evolutionary Adaptations at Species' Range Margins