Evolutionary and Ecological Responses to Anthropogenic Climate Change

This is the authors' abstract. We don't add key points for this paper.

Strategies that enable species to persist in changing environments have historically been divided into ecological (distributional shifts and phenotypic plasticity) and evolutionary (adaptation and gene flow). However, most species will likely need to rely on a combination of approaches to mitigate extinction risks from ongoing climate change. For example, increased temporal variation in climate could favor genotypes with adaptive plasticity. Furthermore, even species capable of tracking their preferred climate via migration will encounter different abiotic and biotic conditions; plasticity and/or adaptation could facilitate establishment and population growth in new geographic ranges. The relative contributions of adaptation, migration, and plasticity to population persistence in a changing world will likely depend on characteristics such as generation time, mating system, dispersal capacity, the strength and direction of selection, the presence of ecologically relevant genetic variation, the extent of genetic correlations among traits, and the genetic architecture of adaptation. Will adaptation keep pace with rapid climate change? Here, we propose hypotheses based on ecological and evolutionary theory, discuss experimental approaches, and review results from studies that have investigated ecological and evolutionary responses to contemporary climate change. We focus our discussion on plants, but owing to the limited number of publications to date that integrate evolutionary and ecological perspectives, we draw from other taxonomic groups as necessary. For species to survive rapid anthropogenic climate change, they must shift their distributions to track preferred conditions (Angert et al., 2011; Chen et al., 2011), adjust their phenotypes via plasticity (Nicotra et al., 2010), and/or adapt to novel stresses (Aitken et al., 2008; Hoffmann and Sgrò, 2011). In most cases, a combination of ecological and evolutionary strategies will be necessary for local and regional persistence in landscapes disturbed by habitat fragmentation, pollution, and invasive species. For example, increased climatic variation (Battisti and Naylor, 2009) could selectively favor phenotypic plasticity (Crozier et al., 2008), which, in turn, could contribute to evolutionary novelty and adaptation (Moczek et al., 2011). Furthermore, many species have already altered their distributions to more poleward and upslope regions because of increasing temperatures (Parmesan and Yohe, 2003; Hickling et al., 2006; Parmesan, 2006; Lenoir et al., 2008; Chen et al., 2011). Migrating populations will undoubtedly encounter novel abiotic and biotic conditions and will need to adjust to different photoperiods, edaphic characteristics, growing season lengths, and altered biotic communities via plasticity and/or adaptation. Gene flow and population admixture could facilitate adaptation by introducing warm- or drought-adapted alleles into populations that are locally adapted to a suite of climatic and nonclimatic variables. Finally, the rate of climate change, combined with the effects of habitat fragmentation, could surpass many species’ abilities to track the climate to which they are currently adapted (Davis and Shaw, 2001). Such species will necessarily have to acclimate or adapt in situ to novel selection pressures or face a heightened probability of extinction (Aitken et al., 2008). Evolution can proceed rapidly (Grant and Grant, 2002; Hairston et al., 2005; Franks et al., 2007), but we know little about the interplay of ecological and evolutionary processes in the context of climate change. Theoretically, adaptation could keep pace with climate change as long as genetic variation, individual fitness, and effective population sizes remain high against a backdrop of strong selection, short generation times, and minimal environmental and demographic stochasticity (Burger and Lynch, 1995; Aitken et al., 2008; Hoffmann and Sgrò, 2011). Will adaptive evolution and/or plasticity allow species to alter their phenotypes fast enough to persist despite rapidly changing conditions (Davis and Shaw, 2001; Franks et al., 2007; Crozier et al., 2008; Teplitsky et al., 2008; Nicotra et al., 2010; Hoffmann and Sgrò, 2011; Shaw and Etterson, 2012)? Can the inheritance of environmentally induced nongenetic modifications alter the rate and direction of species’ evolutionary response to climate change? And can we make robust predictions about the relative contributions of migration, adaptation, and plasticity as a function of attributes of species or the extent of habitat degradation? This review highlights the interdependence of ecological and evolutionary processes to mitigate extinction risks. We discuss hypotheses and approaches that will illuminate the relative roles of migration, phenotypic plasticity, and adaptation in responses to global change (Table I). We encourage collaborations between ecologists and evolutionary biologists to connect studies of phenology, physiology, mating systems, and dispersal with those of ecological genetics/genomics and quantitative genetics. LS, Longitudinal studies; PT, provenance trials; RS, resurrection studies; Sim, simulating predisturbance and postdisturbance conditions experimentally. In some cases, a hypothesis needs to be tested using combined approaches, indicted here by +. LS, Longitudinal studies; PT, provenance trials; RS, resurrection studies; Sim, simulating predisturbance and postdisturbance conditions experimentally. In some cases, a hypothesis needs to be tested using combined approaches, indicted here by +. We may be able to draw from the paleoecological literature to understand extinction risks, migration rates, and potential adaptive responses to climate change (Davis and Shaw, 2001; Leakey and Lau, 2012), especially by focusing on the few geological intervals during which the rate and magnitude of naturally induced climate change were similar to contemporary climate change driven by anthropogenic processes (Willis and MacDonald, 2011). During four geological periods of rapid climate change, macrofossil and pollen records document extensive changes in species’ distribution patterns, but species likely also adapted to novel climates (for review, see Willis and MacDonald, 2011). Some species experienced dramatic reductions in range size and survived rapid bouts of climate change in outlying refugia surrounded by inhospitable habitat (McLachlan et al., 2005; Willis and MacDonald, 2011). Researchers have long turned to the fossil pollen record to examine rates of migration after the last glacial maximum in the late Pleistocene. Palynological evidence suggests that tree species migrated approximately 100 to 1,000 m year−1 after glaciers retreated, a rate that far exceeds average seed dispersal distances measured in natural populations (McLachlan et al., 2005). This discrepancy, known as Reid’s paradox, could result from rare long-distance dispersal events and/or coarse fossil pollen records that do not adequately capture small refugial populations (McLachlan et al., 2005; Magri et al., 2006). Postglacial spread from these refugia would artificially inflate migration rates estimated from the fossil record (McLachlan et al., 2005). Instead, seed dispersal distances and life history characteristics of modern populations are more reliable predictors of the rate of possible range shifts (McLachlan et al., 2005). Today, natural populations face myriad threats that paleocommunities did not experience, including habitat fragmentation and degradation, pollution, and invasive species. These anthropogenic stresses could hinder dispersal (Kremer et al., 2012), alter patterns of selection on complex traits (Cook et al., 2012), and reduce genetic variation (Jump and Peñuelas, 2006; Willi et al., 2007), thereby evolutionary responses to climate change. For these the fossil record likely contemporary extinction risks and potential and the of species to adapt to global change. on our to from we must species’ ecological and evolutionary responses to rapid contemporary climate change. In we hypotheses that (Table I). increased in temperatures and altered However, other abiotic such as and edaphic characteristics, will remain to environments that have et al., likely that climate change will strong selection on complex traits, and that enable and climate change novel Etterson, et al., 2005; Hoffmann and Sgrò, 2011). by climate change could shift adaptive landscapes and alter the magnitude of selection in et al., are likely to to change rapidly novel a for natural populations to adaptation climate and Shaw, 2001; et al., 2005; et al., novel selection will likely reduce and population growth in the short owing to a between average phenotypic and new climate change can reduce and population Willis et al., 2008). populations will be able to in the long will depend on the extent of genetic variation and can be by genetic correlations and among traits and Shaw, 2001). change patterns of local adaptation In genotypes from are into contemporary conditions local genotypes have a their local adaptation. In climatic conditions result in local novel conditions favor genotypes from In the of genotypes the The in would be more complex nonclimatic of selection, such as edaphic also to local adaptation. In that genotypes from of local and could maximum in climates In the long rapid evolution could to adaptation to global change, patterns of local adaptation. In local genotypes are by populations are but not adapted to local conditions et al., 2007; and 2008; studies have the effects of abiotic and biotic of selection on local adaptation, but climate not the that adaptive evolution et al., et al., climatic from other of selection, genotypes may have the in their environments et al., climate change could patterns of local adaptation that likely many to et al., adapted may of extinction as climate change they have climatic and limited dispersal et al., In and phenotypic plasticity could genotypes from the effects of global change et al., We know little about the genetic of local adaptation. to fitness, and climatic variation will allow to changes in climatic adaptation et al., 2005; et al., 2006; et al., For example, and a rapid shift in in from to for the and a regions with climatic adaptation. with changes in the climate that alleles into a genetic response to climate change et al., 2005). In et strong evidence for changes in of in This the potential for such and the for of complex The genetic architecture and of complex traits in climatic adaptation (Aitken et al., 2008). For quantitative traits 2012), approaches could be to changes of small et al., et al., in and will our of climatic adaptation in et al., 2011; et al., and et al., For example, et investigated the genetic of climatic adaptation in by between environmental and variation that were with and to that et al., et a of and Gene with of changes that are with climatic in Such could in climatic adaptation in other but they must be et al., 2011). phenotypic plasticity genotypes to in and environments by to conditions (Moczek et al., 2011). plasticity likely to in the persistence of species in rapidly changing environments (Nicotra et al., studies of populations have extensive plasticity and little adaptive evolution in the context of climate change, that species can alter their phenotypes via plasticity adaptation et al., 2008; et al., of phenotypic plasticity that are for response to global change could be temperatures and et al., In some climatic conditions are to 2007), which could selectively favor plasticity, evolutionary change in climate change et al., 2005; Etterson, 2008; et al., alleles via gene flow et al., 2007), which can genetic variation and adaptive evolution in and or habitat and population et al., 2011). In the context of climate of gene flow could genetic variation and reduce (Kremer et al., 2012), especially in populations gene flow adaptive Furthermore, between and from or more populations could with warm- or drought-adapted alleles in climatic and locally adapted alleles in the admixture could adaptive response to global change in species that are locally adapted to climatic and nonclimatic conditions admixture of conditions in environments that do not In such and pollen may However, climate change from some populations may be adapted to novel conditions long-distance seed dispersal could genetic variation and adaptation as as facilitate migration and of new habitat (Davis and Shaw, 2001; et al., et al., However, the rate of climate change to far the rate of migration for more of the et al., may more track preferred climates short distances upslope or to climatic must to remain the climatic et al., but see Chen et al., 2011). as climate change in situ adaptation could a more for in species that see Chen et al., 2011). The of extinction from climate change likely the range of a species. population sizes and genetic variation can be in the of a species’ range with the in gene flow from to populations and et al., Such gene flow could adaptation to climate change in the of the range or poleward because of the of alleles but adaptation the or because of the of alleles (Aitken et al., 2008; et al., For these populations the could have of local extinction the climate far of genetic and adaptation be most likely in the or of the range et al., 2006; Aitken et al., 2008; et al., We review four for hypotheses about the between ecological and evolutionary processes in species’ responses to climate change (Table I). Longitudinal studies can phenotypic shifts in natural populations and those changes have a genetic et al., However, even records are to the relative contributions of migration, adaptation, phenotypic plasticity, and genetic in changes in studies phenotypes and in natural populations and/or experimental to the extent of phenotypic shifts to climatic phenotypes to climatic that have also genetic variation and selection on traits relevant to adaptation to and phenotypic changes result from migration, plasticity, or genetic adaptation or are a response to conditions et al., 2008; et al., et al., Researchers can the rate of changes could be with genetic et al., Longitudinal studies in could the adaptive potential of populations the range and could populations from the effects of climate change and as experimental studies have studies; genotypes of known can quantitative genetic and robust of the temporal changes in even can of quantitative genetic based on for and studies and in in natural populations of hypotheses to and This most are and the life to on life history and the on the among which can be estimated from studies can genetic and and temporal variation in can and be into to for environmentally induced phenotypic variation in natural populations can to plasticity from adaptation et al., 2008). The few such studies to date that responses to climate change to be by phenotypic plasticity and not genetic adaptation et al., 2008; et al., responses to climate change could also be from shifts in with to and other stresses by global change et al., We know of that changes in in climatic adaptation, such studies have been in et al., 2005; et al., 2006). However, biologists could to changes that have been in For example, the genetic of in and 2010), and of many have effects on in other species et al., 2006). Furthermore, in of the can local adaptation to climate et al., temperatures but remain studies climate change more rapidly in with the and in from the or other other and quantitative are in and studies and for of from or more populations or in situ could result in phenotypic change with natural selection and by adaptive shifts in on population genetic and migration rates could illuminate phenotypic change results from of local genotypes by which are already adapted to or conditions; in situ adaptive evolution from genetic or gene flow and of warm- or drought-adapted alleles from and we would to see shifts in and adaptive the patterns of variation would more patterns from However, in postdisturbance populations could be to nonclimatic local In rapid in situ adaptive evolution that are the of climate selection and and change a of admixture we a of will with even in to population and migration rates more et al., we have that the of and rapid on similar approaches in populations et al., et al., the for genetic responses to climate change. Longitudinal studies can a of et al., phenotypic and genetic records are not currently for most species. of populations many will be necessary The approaches will on and genetic responses to climate change in a more and in from and after environmental change, Franks et rapid evolution in response to and et evolution in response to changing a to the of for studies of the evolutionary response to temporal variation, especially in the context of climate change (for review, see Shaw and Etterson, This resurrection could also be to species the of to the need to for traits and/or alter are as the studies can the rate of the of climate the genetic of rapid adaptation to with populations and between plasticity and and hypotheses about environmental on complex traits and plasticity and see Franks et al., 2007; et al., Shaw and Etterson, These could also populations can to rely on new for life history as and other environmental from the and after population studies and would allow to are in or from population admixture and Finally, resurrection studies that from the range into environments could examine local adaptation and range and This can be long with minimal selection and robust sizes of a resurrection not could on For example, Willis and on a record of and patterns of species in natural communities of which were by in the and between and a to the response to climate change and a strong in among species that were to adjust their (Willis et al., 2008). climate change can have for species that are of or adaptive responses such as of the growing and change and and which can result in patterns of adaptation to local climatic conditions et al., 2007; and 2008; et al., 2011). Researchers can natural climatic variation these to adaptation in the context of global change and Shaw, 2001; et al., 2010; et al., studies that changing the biotic and the of experimental into the in to the response to selection and Etterson, by enable of adaptation in the context of climate change Aitken et al., 2008; et al., These genotypes from many populations climatic to in thereby a range of would be in In provenance can the of et al., 2010), in which as the climate to would have phenotypes and with genotypes from hypothesis In with population genetic and provenance be able to between gene flow and adaptive evolution can be as a function of climatic in the and the provenance of a and that genotypes from populations in the of the range of the in et of genotypes in their provenance with the genotypes other and that climate change will patterns of local adaptation in the genotypes from the range will have growth patterns in their the of will be of et al., This also that a on the of experimental did genetic effects et al., 2010), the hypothesis that phenotypic plasticity will a in responses to global change. Researchers can experimental that conditions and that contemporary environments et al., that genotypes of known from populations the range of a can of the hypotheses in and Lau, 2012), especially combined with provenance or of and genotypes in selection can also be to adaptation to climate change and many will be et al., growing season date in and and/or based on for a et al., may be to climates because of in and Etterson, 2012), can the effects of different of selection on the evolution of complex traits, the effects of these and more climatic of the need for could and but reductions in from and temperatures could those effects and 2005; et al., 2006; et al., in environmental can and climatic conditions to adaptation to climate in from other environmental However, environments do not the of abiotic and biotic conditions that species in and Lau, studies 2008), thereby the rate of species’ evolutionary responses to global change, experimental studies be in natural capture variation and events and can patterns responses to variation in et al., 2006). few evolutionary genetic studies have climatic in the results to date that the response to not genetic (for review, see Leakey and Lau, a need for that genotypes to different climatic for biologists on ongoing such as the the et al., to the evolutionary of climate change and In have been for many of populations from and can be in of the to hypotheses and and suggests that shifts in et al., and similar responses to experimental and and to natural of variation in climate and our predictions of ecological and evolutionary responses to anthropogenic climate change from studies that integrate with approaches and phenotypes as a function of climatic the of of et al., The most of the evolutionary and ecological responses to climate change will from climatic conditions can be in with provenance in the context of natural climatic to hypothesis and limited genetic variation adaptation, especially in the of the range can the of admixture by from between populations different with the of and quantitative as as in and we have potential to our of ecological and evolutionary responses to climate change. The discussion highlights which could are not of traits that can in response to novel climates and Shaw, natural selection on responses to climate change could be or even novel selection traits in 2008). In a of to of the and Shaw that genetic correlations among traits adaptation to even traits genetic evolution on genetic among traits, which can be to selection et al., 2008). The potential for adaptive evolution may from from studies of or a few traits and Shaw, 2001). of evolutionary responses to global change, we that traits with adaptation to climate and other abiotic and biotic of selection (Table for a see et al., 2011). The here are by The here are by a species will adapt to changing climatic conditions could in on life history mating system, generation time, and et al., 2010; et al., However, make to which traits or of traits will be adaptive in such a as global change. For example, and will likely adaptive responses to climate change but habitat fragmentation may genetic variation more rapidly in species et al., 2008). species have for rapid adaptive responses to climate change, high genetic variation, extensive gene and limited et al., but a suggests that mating not patterns of local adaptation in contemporary environments modifications could facilitate adaptive responses in species with little genetic variation, such as and et al., 2008; and Furthermore, may more from of and 2011). will likely on a complex interplay between genetic variation, the of new genetic variation, and effective population seed and generation are complex traits that could also adaptive responses to changing For example, long-distance dispersal could enable adaptation and migration (Kremer et al., in a seed could of genetic to habitat fragmentation, but may rapid evolution by introducing genotypes that were adapted to Finally, have gene flow and seed dispersal potential species with similar mating and increasing the rates of adaptation and migration in the context of climate change. However, the long generation of could adaptation, and rates of could local populations to pollen and seed et al., plasticity as a but can also such that the experienced by the in the et al., plasticity by nongenetic of such as the of variation and from to (for review, see and modifications have been to ecologically relevant phenotypic plasticity in natural populations of and and of in et al., These environmentally induced modifications can be et al., 2006; and and could in species responses to climatic change et al., 2008; and studies have to the between inheritance and environmental change, we know that increased temperatures can have effects on rates, seed and et al., suggests that inheritance can reduce with responses to environmental et al., and can novel phenotypic variation into populations with little genetic and that plasticity, by nongenetic can the rate and direction of adaptation et al., 2008; et al., studies that track the of modifications be combined with selection to the of these modifications on evolutionary change and 2011; and Such studies the effects of modifications on the to which environmental change and the potential for selection to on and 2011). to natural variation of inheritance in and and et al., can many of the approaches in for evolutionary can be to studies of variation, including for population and quantitative for to et al., 2008; and The between and genetic variation from to a for 2006). can for the effects of genetic variation by focusing on species that genetic variation, populations and/or by natural or of induced changes in by the of or et al., 2008; and for genetic between will between environmental variation, plasticity, and evolutionary responses to environmental change. the of as or could the evolutionary of modifications et al., 2011; and The effects of climate change be in from pollution, habitat fragmentation, and other anthropogenic et al., fragmentation effective population sizes and geographic genetic variation et al., 2007; et al., 2008; et al., can species’ abilities to track climate via migration and gene flow among populations (Kremer et al., 2012), genetic habitat fragmentation likely adaptation to novel climates Furthermore, shifts in traits and by genetic and/or could extinction risks in studies of the genetic of habitat fragmentation have on et al., 2008). However, not genetic variation in traits et al., and few studies have fragmentation variation in complex traits to natural selection et al., studies genetic variation in ecologically relevant traits among populations that in the extent of and population size et al., populations adaptive genetic variation limited of and evolution in small and populations et al., fragmentation evolutionary potential in the context of climate change? These remain likely because they to genetic variation and selection on complex traits the effects of geographic and population size However, such studies would a of about responses to novel stresses with anthropogenic change. of to the adaptive potential of populations In studies from populations that in size and geographic here by of genetic as a function of effective population size and geographic This most studies of the genetic of habitat fragmentation have In as as genetic variation in ecologically relevant and as a function of effective population geographic or genetic and the habitat fragmentation These could population genetic Finally, in genotypes to contemporary conditions and and responses to in could fitness, and other response as a function of population size and genetic The of climate change could be more in in change threats for and (Battisti and Naylor, et al., of the effects of climate change on populations and communities to evolutionary responses and that populations will shifts see et al., ecological and evolutionary responses to climate change will enable (Aitken et al., 2008; et al., For example, and propose to including habitat for genetic and adaptive with migration as a last This review on evolutionary responses of to changing abiotic However, climate change will to alter biotic communities as distribution patterns change, invasive species more and shifts in alter species et al., et al., species in their responses to climate change (Davis and Shaw, 2001). the evolutionary responses of species to their changing biotic but will likely be more complex responses to abiotic Finally, the of studies of responses to climate change have on systems, despite of and novel climates in 2007; et al., 2007; and Naylor, In with limited and temporal variation in climate genetic variation in complex traits with adaptation to climate et al., We encourage collaborations that with the of ecological and evolutionary responses to climate change in a of from to and We are to and for on and to for