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Evolution in Response to Climate Change
Evolution in Response to Climate Change Julie R Etterson, University of Minnesota, Duluth, MN, USA Ruth G Shaw, University of Minnesota, St Paul, MN, USA r 2013 Elsevier Inc. All rights reserved.
Glossary Adaptation Increase in fitness due to response to natural selection. Gene flow Dispersal of individuals (or pollen) between populations, resulting in a genetic contribution from one population to another. Genetic drift Random change in the frequency of alleles or genotypes within a population. Genetic variation Variation in traits attributable to genetic differences among individuals in a population. Habitat fragmentation Subdivision of wild habitat, coupled with conversion of wild habitat for use by humans (e.g., agriculture, urbanization). Heritability Genetic variation expressed as a proportion of the overall variance in a trait. Inbreeding Mating between relatives. This results in progeny that carry two copies of the same allele at many loci throughout the genome.
Introduction
Evolution is Complex
Research on evolutionary responses of wild populations to climate change has been stimulated by accumulating evidence demonstrating exceptional rapidity of recent climate change and predictions of rapid change in climate into the future. However, it is challenging to demonstrate empirically that observed changes in wild organisms are due to changing climate per se because of the complex dynamics of both climate and evolution.
Climate is Complex Climate comprises many attributes (i.e., temperature maxima and minima, rainfall, humidity, insolation, all varying over the seasons) and is manifest over extended periods, rather than instantaneously. Consequently, climate cannot be imposed or manipulated experimentally, though individual components of it can be, on a limited spatial scale. In nature, climatic variation is correlated with other aspects of the environment; for example, temperature regimes vary latitudinally along with photoperiod; characteristics of soils vary, in part due to the effects of water percolating through them (Baldwin et al., 1938). Moreover, erratic variability in climate is superimposed on the regularity of annual climate cycles; forecasts indicate that climate variability will increase, such that extremes occur more frequently (Alley et al., 2007).
Encyclopedia of Biodiversity, Volume 3
Mutation A heritable change in the nucleotide sequence of an organism. Natural selection Variation among individuals in their contribution of offspring to the next generation. To the extent that this variation in offspring number is associated with genetic differences among individuals in the population, natural selection results in change in the population’s genetic composition and tends to increase its average fitness. Phenotypic plasticity Response of traits to the environment in which an organism develops. Provenance test An experiment, particularly in forestry, in which plants from different source locations are grown together in common conditions (also referred to as common gardens), often in multiple locations, as a basis for assessing genetically based differences in trait values.
The complexity of climate is matched by that of evolution, defined as genetic change in populations over generations. Genetic change results from any or all of four evolutionary processes: natural selection, genetic drift, mutation, and gene flow between populations that have diverged genetically (Hartl and Clark, 2006). However, some changes that are observed as environment changes, for example, in flowering time, or migration date, may reflect direct effects of environment on individuals during their development, i.e., phenotypic plasticity (Bradshaw, 1965). Thus, conclusive assessment or prediction of evolutionary change entails multigenerational studies designed to distinguish genetic from environmental responses. Evolutionary theory, developed over nearly a century, ameliorates these challenges by grounding and guiding evolutionary explanation and prediction.
Populations Have Evolved in Response to Climate Change in the Past Despite the inherent complexities of both climate and evolution, which impose formidable challenges to study of evolutionary responses to climate change, it is well established that populations have adapted to different climates in the past. Climate has resulted in evolutionary convergence of morphological and physiological traits in unrelated taxa as illustrated by the increase in wind pollination during the arid Eocene period (Crepet, 1989) and rise of C4 photosynthesis during a period of low CO2 concentration during the Miocene
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(Ehleringer et al., 1991). It is clear that on a geological time scale, natural selection due to climate has powerfully shaped the attributes of organisms.
Populations Will Evolve in Response to Climate Change in the Future As climate continues to change, natural selection is expected to change such that different trait values will be favored, compared to the past or present. For example, natural selection may favor traits associated with earlier phenology or enhanced tolerance of drought or heat. If populations harbor genetic variation for traits under selection (and other genetic and demographic aspects of the population are conducive to evolutionary change, see Evolutionary Rates), populations are expected to adapt in response. Beyond altering natural selection, changes in climate are also likely to influence other evolutionary processes such as gene flow, genetic drift, and inbreeding.
What is this Article About? Here the authors review basic concepts in evolutionary genetics with an emphasis on how they pertain to studies of the adaptation to climate change. They focus on evolutionary responses of wild populations inherently subject to the fundamental evolutionary processes; they do not consider domesticated populations, in which genetic change is dominated by decisions of breeders. The authors provide an overview of approaches that have been employed to elucidate adaptive evolution in natural populations in response to both geographical variation in climate in the past and to contemporary climate change. These approaches include observational studies conducted across spatial and temporal gradients, experimental manipulation of genetic and environmental factors, prediction of future evolution based on standing levels of genetic variation and selection gradients, and simulation modeling of evolutionary change.
Overview of Evolutionary Genetics Populations are constantly changing. An increasing number of studies have documented changes in natural populations, even over a few generations (Grant and Grant, 1993; Reznick et al., 1995; Bradshaw and Holzapfel, 2001; Re´ale et al., 2003; Franks et al., 2007). However, it is important to recognize that not all changes that have been observed in recent decades (e.g., Walther et al., 2002) in natural populations reflect evolutionary responses to natural selection. A clear distinction needs to be made between ‘‘environmental response’’ and ‘‘evolutionary response.’’
Environmental versus Evolutionary Response Environmental response of organismal traits, or phenotypic plasticity, reflects the direct dependence of organisms’ physiology, growth, development, and behavior on the environmental conditions they experience through their lifetimes (Bradshaw, 1965). Plastic responses do not involve changes in
the genetic composition of a population but manifest environmental influences on the expression of genes (e.g., flowering time, Aikawa et al., 2010). In contrast, evolutionary change is the change over generations in the genetic composition of a population. All populations are continually subject to evolutionary change. It results from several processes, including natural selection, i.e., variation among genotypes in survival or reproductive success. Natural selection is the basis for adaptation. Genotypes that express adaptive phenotypes make a greater genetic contribution to the subsequent generation; in this way, alleles that confer higher fitness in a given generation gain in frequency in the population. Natural selection may also favor plasticity that maintains high fitness in a variable environment. For example, a genotype that produces thin leaves in mesic conditions but thicker leaves when it develops in more arid conditions may have a survival or reproductive advantage over genotypes that do not respond in this way. If there is variation among genotypes in their phenotypic plasticity and this variation is under selection, plasticity itself can evolve (Via, 1993). In the context of climate change, phenotypic changes such as timing of flowering and breeding that correspond statistically with recent climatic trends are well documented (Parmesan and Yohe, 2003). Observation of such changes does not reveal the basis of these responses, whether plasticity in response to immediate environmental condition, adaptive evolution in response to selection mediated by environmental change, or a combination of these. Phenotypic plasticity may buffer populations against natural selection in the short term. However, the limits of phenotypic plasticity in maintaining fitness over a range of environments are poorly understood, and, over the long term, ongoing climate change is expected to exceed those limits (DeWitt et al., 1998). Thus, as climate continues to change, it is likely that natural selection will alter plasticity of traits as well as their expression in particular environments, given climate model predictions that include both directional change and increased variability.
What is Natural Selection? Natural selection occurs when genotypes in a population differ in fitness, their contribution of progeny, and the genes they carry, to subsequent generations. Over generations, natural selection is expected to increase the average fitness of populations in the environments in which they undergo selection. This process of adaptive evolution proceeds over generations at a rate that depends on the severity of genetic selection, the genotypic variation in fitness. Climate conditions that are novel relative to previous ones at a particular location are likely to impose a typically strong directional selection on traits, such as rooting depth, that are related to survival in dry conditions. This would be expected even if climatic changes were smooth. However, the prediction that climate is becoming more erratic implies that bouts of intense selection in one direction (e.g., favoring greater drought tolerance) will be interspersed with weaker selection or even selection in the opposite direction. Evolutionary dynamics may be governed by such extreme selective events (Grant and Grant, 2002; Gutschick and BassiriRad, 2003).
Evolution in Response to Climate Change Evolutionary Rates
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relative fitness and traits (Price, 1970):
The rate of evolutionary response to selection depends on both genetic variation and environmental conditions and is most simply illustrated by the breeder’s equation (1). The expected amount of phenotypic change (R) in a single trait per generation in response to selection depends on the strength of selection on that trait as measured by the selection differential (S), a statistical measure of the association between fitness and trait values, and also on genetic variation for the trait as expressed by heritability (h2): R ¼ h2 S
½1
Heritability (h2) estimates the fraction of the total phenotypic variance (VP) due to additive genetic variance (VA): h2 ¼ VA =VP
½2
VA is the variance in a trait that is attributable to segregation of alleles at all the genes that influence that trait, and the resemblance of relatives due to sharing of alleles at all these genes is proportional to h2 (Falconer and MacKay, 1996). VA, VP, and S are not static quantities. The expression of additive genetic variance and the total phenotypic variance depend on the immediate environmental conditions, as does the selection differential. Thus, estimates of heritability and selection are context dependent and are applicable to prediction of selection only in the specific environment for which they have been estimated. The single-trait breeder’s equation is not adequate to describe response to selection when multiple traits are under selection and are genetically correlated with each other. Genetic covariance between pairs of traits, each subject to selection, can promote the response of each to selection, if, for example, the sign of the genetic covariance is positive and both traits are selected in the same direction. Conversely, a positive genetic covariance between traits impedes response of both traits to selection if higher values of one trait and lower values of the other are associated with higher fitness. The genetic variances of traits and the genetic covariances between pairs of traits depend on direct effects of environment on organisms and the traits they express; genetic variation in traits and fitness may be reduced (Hoffmann and Parsons, 1991) or enhanced (e.g., Shaw et al., 1995) in harsh environmental conditions. Genetic correlations between traits can be included in predictions of selection response using a multivariate extension of the breeder’s equation: Dz ¼ Gb
½3
where the predicted change in the means of a set of traits (expressed in a vector, Dz) across one generation depends on the additive genetic variance–covariance matrix (G) and the vector of selection gradients (b) (Lande, 1979). As in eqn [1], use of this expression to obtain predictions of selection response requires taking the product of two estimates, each of which has substantial statistical uncertainty due to sampling and measurement error. Thus, interpretation is not straightforward. Alternatively, the response to selection can be estimated directly as the additive genetic covariance between
Dz ¼ CovA ½w,z
½4
where w is individual relative fitness (absolute fitness divided by mean fitness), and z is the vector of trait values (Shaw and Shaw, 1994; Etterson and Shaw, 2001; Hadfield et al., 2010).
What Processes Influence Genetic (co)variance? As with additive genetic variances, additive genetic covariances also depend on a population’s genetic composition, and strong selection over the extended period of climate change may radically deplete genetic variation. Spontaneous mutation steadily augments genetic variation; under changing conditions, novel mutations may more likely contribute to ongoing adaptation. Furthermore, influx of genes from genetically divergent populations increases genetic variation. Consequently, G (eqn [3]), which governs the immediate response to selection, i.e., from the current generation to the next, is expected to change with ongoing climate change, though the net effect of all the processes that influence G is not readily predictable. In populations where climatic conditions become so severe that population size drops dramatically, genetic variation is expected to decline due to genetic drift. By this process of random sampling, genes that could contribute to adaptation can be lost (e.g., Weber and Diggins, 1990). Moreover, as populations decline in size, inbreeding increases, reducing fitness itself (i.e., inbreeding depression) further impairing populations’ capacity for increase. Inbreeding may also slow the response to selection (e.g., Shaw et al., 1998). Moreover, the number of new mutations in a population declines directly with the population’s size, with the consequence that particular mutations, for example, those that could support adaptation to changing climate, are less likely to arise. These considerations underscore the intimate connection between the demography of populations and changes in their genetic composition. Evolutionary theory before 1990 tended to ignore this connection, but such simplification is especially likely to mislead in circumstances when conditions are so severe that populations become small and are at risk of extirpation. In many cases, such populations are likely to die out. For others, immigration can play the important demographic role of increasing the size of a population, enhancing its chance of persisting, in addition to contributing to its genetic variation (Holt and Gomulkiewicz, 1997).
Evolution of Plasticity The tendency for natural selection to favor adaptive plastic responses will depend on the extent to which climate increases in variability. In the simplest case, if climates were to change monotonically (e.g., becoming progressively warmer or drier), then natural selection may favor adaptive evolution via fixed genetic changes that result, for example, in earlier breeding or greater thermal/drought tolerance. However, in the more realistic case in which climate variability increases (Alley et al., 2007), and hence variability in natural selection does also, then adaptation involving plasticity may enhance fitness
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across a range of environments. However, reversals in genotypic fitness, either within the lifetime of an organism or between generations, are expected to impede evolutionary increase in population mean fitness because genotypes with high fitness under both sets of conditions will be rare (Via and Lande, 1985; Gillespie and Turelli, 1989; Van Tienderen, 1991; Gomulkiewicz and Kirkpatrick, 1992; Gavrilets and Scheiner, 1993a, b). Adaptive plasticity is also less likely to evolve in a highly erratic and unpredictable climate marked by extreme events.
Approaches to Understanding Evolution in Response to Climate Change Adaptation to Climate in the Past Past evolution in response to climate is evidenced by the current adaptation of organisms to their home environments, encompassing climate, among many other aspects. A high degree of adaptation to an environment is reflected in high fitness (comprising individual survival and reproduction) that contributes to persistence of a population in that environment. This implies that, in previous generations, the population has undergone natural selection in those (or similar) conditions and, as a consequence, its genetic composition has changed, with increased frequency of genes conferring greater fitness than would otherwise be the case.
to genetic differentiation, phenotypic plasticity, or some combination of these can be ascertained through ‘‘common garden’’ experiments in which populations are sampled from an environmental gradient and reared in common conditions (e.g., Reinartz, 1984; Lacey, 1988). By subjecting the populations to the same environment, such experiments demonstrate that differences detected among them in morphology, physiology, and phenology, in the common garden setting, must be genetically based. Furthermore, if this differentiation is related to the gradient from which they were sampled, they will retain clinal patterns in a common environment (e.g., Etterson, 2004a). Clinal patterns that disappear in a common garden can be attributed to phenotypic plasticity (e.g., Maherali et al., 2002). Expanded forms of the common garden approach involve multiple growing locations, including reciprocal transplant studies (Clausen et al., 1940; Etterson, 2004a, b) and provenance trials (e.g., Rehfeldt et al., 1999). These experimental designs make possible comparisons of the relative adaptation of populations under different climatic conditions, and in relation to the climates at the locations from which the populations were drawn. Manipulation of some particular aspect of climate as an added experimental component of a common garden may yield yet stronger evidence of past adaptation to prevailing climatic conditions.
Observations Over Time Range Limits and Climate Variables The limits of species’ ranges commonly coincide with abrupt spatial gradients in climatic attributes, and the geographic extent of a species’ range can sometimes be predicted with high confidence from climate data taken in a subset of its range (Peterson et al., 1999). The geographic ranges of species have shifted during past periods of climate change and shifts in range are ongoing. Shifts of the range of species may be an important component of the biological response to climate change in the future. However, it is not clear that range shifts of populations will proceed at sufficient rates, such that they will be subject to similar climatic conditions as climate changes. For example, it is often suggested that severe fragmentation of contemporary habitat is likely to impede dispersal. Moreover, interactions within and between species may thwart establishment of a population in locations beyond the current range where climate has become suitable for it. Beyond the role of geographic shift in a species range, the evolution of range limits is expected, even in the absence of climate change (Kirkpatrick and Barton, 1997).
Geographic Variation among Populations within a Species Species that occur across environmental gradients frequently express clinal patterns in phenotype that may suggest underlying local adaptation. However, these patterns do not necessarily reflect genetic differentiation, but may result from phenotypic plasticity, which may or may not be adaptive. The extent to which clinal patterns in phenotype can be attributed
Evolutionary response to climate change has already been documented for a few wild organisms for which long-term studies of field populations have been conducted. For example, over the past 30 years mosquitoes that breed in pitcher plants in the eastern US have evolved different genetically based photoperiodic cues for breaking dormancy that correspond to increases in the length of the growing season in recent decades (Bradshaw and Holzapfel, 2006). In Australia, 20 years of temporal sampling of fruit fly populations has demonstrated latitudinal shifts of clinal variation of genetic traits (Umina et al., 2005). Rapid evolution of clinal variation has also been observed for several invasive species since the time of establishment (e.g., Huey et al., 2000). It has also been inferred that the timing of breeding has evolved in a population of red squirrels in Canada. In the last decade, spruce trees have been producing their cones progressively earlier (Re´ale et al., 2003), and this has exerted selection on the squirrel population resulting in earlier breeding. By tracing the inheritance of timing of breeding from parents to offspring for several generations, these researchers undertook to distinguish genetic change from phenotypic plasticity and ultimately attributed the observed changes to both. The authors note, however, that Hadfield et al. (2010) have called the conclusions of this and some other studies into question because the statistical methods used do not fully account for sampling variance. Given the difficulty in obtaining high-quality empirical data sets of this kind that are sufficiently large to allow robust methods of analysis, it is not surprising that there are few unequivocal examples of genetically based evolution in response to contemporary climate change (Gienapp et al., 2008).
Evolution in Response to Climate Change Resurrection Ecology In a few cases, direct demonstration of the nature of contemporary change in wild organisms has been possible because propagules (e.g., seeds in tundra soil or eggs in lake sediments) were recoverable or fortuitously available such that ancestors could be revived and compared side-by-side with their descendants (Bennington et al., 1991; Vavrek et al., 1991; Hairston et al., 1999; Kerfoot et al., 1999; Franks et al., 2007). This ‘‘resurrection approach’’ (Davis et al., 2005; Franks et al., 2008) has permitted phenotypic and genetic comparisons of populations representing different times. The work of Franks et al. (2007) illustrates this approach. They compared the date of first flower of plants that were revived from seeds stored in 1997 with that of plants grown from the seed of their descendants sampled in 2004 following an intervening drought. This comparison yielded estimates of rates of evolution and comparison with changes predicted from quantitative genetics theory.
Experimental Manipulation of Population Genetics Artificial selection involves experimental imposition of selection to answer questions about potential rates of evolutionary change. In practice, a researcher selects from a population individuals that express phenotypes of interest, for example, drought tolerance or earlier flowering. The selected individuals are interbred with the expectation that, if the trait is heritable, its phenotypic mean will differ in the offspring of the subsequent generation. From eqn [1] we can see that if the strength of selection (S) is experimentally determined and the response to selection (R) is observed, we can estimate the realized heritability (h2) of the trait of interest. An alternative approach is to expose a population to an environment (e.g., higher temperatures) in which genetic variation in fitness is expressed, such that natural selection proceeds (Bennett et al., 1992). Following several to many generations, fitness and other traits are compared between the selected and control populations to determine the extent of evolutionary change. Experimental evolution by either of these approaches may demonstrate evolutionary change in numerous traits. Information obtained from studies of experimental evolution has improved our understanding of biotic response to climate change in numerous ways. For example, artificial selection studies have shown that it is possible that shifts in flowering time in herbaceous plant species that have been observed in nature (Parmesan and Yohe, 2003) may be due, in part, to evolutionary change (Burgess et al., 2007). In bacteria, studies where organisms evolved under experimental conditions have resulted in dramatic adaptive evolution in thermal tolerance (Lenski, 2001). It is particularly notable that adaptation proceeded in populations that initially lacked genetic variation; thus the adaptation that occurred depended entirely on newly arising mutations, and proceeded even under conditions of fluctuating selection. Mongold et al. (1999) have further shown that genes that can support adaptation beyond the presumed lethal thermal limit of E. coli fail to increase in frequency in competitive conditions. Consequently, only when populations decline in abundance does
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adaptation to such extreme thermal conditions proceed, a clear example of the intimate connection between demographic and genetic change. In contrast to the previous examples, some experiments to evaluate potential for adaptive evolution in response to aspects of global change have detected only limited evolutionary responses. Potvin and Tousignant (1996) manipulated both temperature and CO2 concentration and found that responses of wild mustard following seven generations in those conditions were primarily through nonadaptive plasticity. In summary, experimental evolution is a powerful approach that will continue to elucidate the rate of evolutionary change, the presence of genetic variation for traits that are under selection, and the role of genetic correlations in evolutionary change.
Prediction of Future Evolutionary Trajectories To predict adaptation in response to climate change, we need estimates for three fundamental pieces of information: the strength and direction of selection in future climates, the genetic variances of traits that are under selection in altered environments, and the extent to which these traits are genetically correlated with other traits. Selection regimes currently impinging on populations at lower elevation or latitude may simply shift to higher elevations or latitudes as climate warms and the geographical ranges of species track these shifts. However, populations may change in more complex ways because the ecological context, both abiotic and biotic, will be altered. Paleoecologists, having extensively studied assemblages of species in the past via the pollen record, have frequently noted that these assemblages often do not have present-day analogs, which suggests that environmental conditions are not closely replicated in different eras. A direct way to assess trends in selection is to do phenotypic selection analyses on data collected from longterm studies of field populations. However, data sets that are complete enough to document such temporal changes in selection on wild populations are rare (but see Grant and Grant, 1995). An alternative approach is to compare natural selection in current environments to selection in experimental conditions similar to those predicted for the future. However, most studies that have manipulated environmental conditions, such as temperature, precipitation, and CO2 have focused on changes in species composition rather than on patterns of natural selection, although there are a few exceptions (Totland, 1999). Insight into temporal changes in selection may also be obtained by characterizing changes in selection along environmental gradients that encompass a range of conditions similar to those predicted for a given location in the future (i.e., a chronosequence, Etterson, 2004a). This approach may provide an incomplete picture of future selection because native species composition will also be altered by climate change and invasive species, pests, and diseases may invade new territories and alter patterns of selection. Furthermore, patterns of selection may be more erratic in the future if climates become more prone to extreme events such as drought, heavy precipitation, heat waves, and intense tropical cyclones (Alley et al., 2007).
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Theory for Evolutionary Response to Changing Environment The persistence of populations in changing environments depends on both evolution and demography. Theory that couples evolutionary and demographic dynamics of closed populations has shown that even if adaptive responses are possible, densities may fall below some critical level such that populations are susceptible to extinction by stochastic processes (Bu¨rger and Lynch, 1995; Gomulkiewicz and Holt, 1995). Genetic variation in a trait subject to changing selection as environment changes can enhance the persistence of populations in a changing environment whether the population shifts in its range in conjunction with the changing environment (Pease et al., 1989) or not (Bu¨rger and Lynch, 1995). Levels of genetic variation and therefore, the potential for adaptive evolution, are not likely to be uniform among populations across the species range (Antonovics, 1976; Lenormand, 2002). As populations become increasingly fragmented, with reduced dispersal among subpopulations, their potential for local adaptation is expected to increase (Dickinson and Antonovics, 1973; Garcia-Ramos and Kirkpatrick, 1997). Nevertheless, even if marginal populations are not swamped by gene flow from central populations, adaptive evolution may be slowed due to strong selection causing genetic variance to be depleted (Fisher, 1930). Genetic drift may also erode genetic diversity, especially in small and isolated populations near the periphery of the species range or in remnant populations (Wright, 1931; Nei, 1973). Thus, fitness may be positively or negatively influenced by gene flow between populations. Adaptation may be more rapid with gene flow, both because it increases genetic variation in traits subject to selection (Swindell and Bouzat, 2006) and because it impedes genetic drift (Lopez et al., 2009), even in an environment that is constant through time. In populations spanning gradual environmental gradients, gene flow between adjacent populations is not expected to inhibit local adaptation because populations are similarly adapted. Marginal populations evolve in response to extreme conditions expanding their tolerance limits and geographic ranges. However, if the environmental gradient is steep, the process of local adaptation is swamped by gene flow between populations that are adapted to substantially different environments (Kirkpatrick and Barton, 1997).
Summary Evolution proceeds unceasingly in all biological populations. Rapid adaptation to human-mediated environmental change was evident long before climate warming became apparent. Consequently, there is no doubt that natural populations will continue to evolve and, in particular, that adaptation to changing climate is possible, in principle. However, it remains unclear how the several evolutionary processes – natural selection, mutation, gene flow, and genetic drift – will jointly alter any single population or the biota collectively. Even though natural selection is likely to proceed, there is insufficient understanding to predict for how many species and which species the rate and extent of adaptation will be
adequate to support persistence, given the very high rates of environmental change expected. Such predictions will require further empirical investigation (experimental, as well as observational) of genetic variation and natural selection, directly accounting for increasing variability of climate. Moreover, the remaining evolutionary processes and their interplay, all of which are sensitive to demographic aspects of populations, are expected to bear importantly on genetic change in nature. Research that accounts for these processes, as well as natural selection, will yield more reliable prediction of evolution and species persistence in the face of changing climate.
See also: Climate Change and Extinctions. Climate Change and Wild Species. Plant Phenology Changes and Climate Change
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Glossary Adaptation Increase in fitness due to response to natural selection. Gene flow Dispersal of individuals (or pollen) between populations, resulting in a genetic contribution from one population to another. Genetic drift Random change in the frequency of alleles or genotypes within a population. Genetic variation Variation in traits attributable to genetic differences among individuals in a population. Habitat fragmentation Subdivision of wild habitat, coupled with conversion of wild habitat for use by humans (e.g., agriculture, urbanization). Heritability Genetic variation expressed as a proportion of the overall variance in a trait. Inbreeding Mating between relatives. This results in progeny that carry two copies of the same allele at many loci throughout the genome.
Introduction
Evolution is Complex
Research on evolutionary responses of wild populations to climate change has been stimulated by accumulating evidence demonstrating exceptional rapidity of recent climate change and predictions of rapid change in climate into the future. However, it is challenging to demonstrate empirically that observed changes in wild organisms are due to changing climate per se because of the complex dynamics of both climate and evolution.
Climate is Complex Climate comprises many attributes (i.e., temperature maxima and minima, rainfall, humidity, insolation, all varying over the seasons) and is manifest over extended periods, rather than instantaneously. Consequently, climate cannot be imposed or manipulated experimentally, though individual components of it can be, on a limited spatial scale. In nature, climatic variation is correlated with other aspects of the environment; for example, temperature regimes vary latitudinally along with photoperiod; characteristics of soils vary, in part due to the effects of water percolating through them (Baldwin et al., 1938). Moreover, erratic variability in climate is superimposed on the regularity of annual climate cycles; forecasts indicate that climate variability will increase, such that extremes occur more frequently (Alley et al., 2007).
Encyclopedia of Biodiversity, Volume 3
Mutation A heritable change in the nucleotide sequence of an organism. Natural selection Variation among individuals in their contribution of offspring to the next generation. To the extent that this variation in offspring number is associated with genetic differences among individuals in the population, natural selection results in change in the population’s genetic composition and tends to increase its average fitness. Phenotypic plasticity Response of traits to the environment in which an organism develops. Provenance test An experiment, particularly in forestry, in which plants from different source locations are grown together in common conditions (also referred to as common gardens), often in multiple locations, as a basis for assessing genetically based differences in trait values.
The complexity of climate is matched by that of evolution, defined as genetic change in populations over generations. Genetic change results from any or all of four evolutionary processes: natural selection, genetic drift, mutation, and gene flow between populations that have diverged genetically (Hartl and Clark, 2006). However, some changes that are observed as environment changes, for example, in flowering time, or migration date, may reflect direct effects of environment on individuals during their development, i.e., phenotypic plasticity (Bradshaw, 1965). Thus, conclusive assessment or prediction of evolutionary change entails multigenerational studies designed to distinguish genetic from environmental responses. Evolutionary theory, developed over nearly a century, ameliorates these challenges by grounding and guiding evolutionary explanation and prediction.
Populations Have Evolved in Response to Climate Change in the Past Despite the inherent complexities of both climate and evolution, which impose formidable challenges to study of evolutionary responses to climate change, it is well established that populations have adapted to different climates in the past. Climate has resulted in evolutionary convergence of morphological and physiological traits in unrelated taxa as illustrated by the increase in wind pollination during the arid Eocene period (Crepet, 1989) and rise of C4 photosynthesis during a period of low CO2 concentration during the Miocene
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(Ehleringer et al., 1991). It is clear that on a geological time scale, natural selection due to climate has powerfully shaped the attributes of organisms.
Populations Will Evolve in Response to Climate Change in the Future As climate continues to change, natural selection is expected to change such that different trait values will be favored, compared to the past or present. For example, natural selection may favor traits associated with earlier phenology or enhanced tolerance of drought or heat. If populations harbor genetic variation for traits under selection (and other genetic and demographic aspects of the population are conducive to evolutionary change, see Evolutionary Rates), populations are expected to adapt in response. Beyond altering natural selection, changes in climate are also likely to influence other evolutionary processes such as gene flow, genetic drift, and inbreeding.
What is this Article About? Here the authors review basic concepts in evolutionary genetics with an emphasis on how they pertain to studies of the adaptation to climate change. They focus on evolutionary responses of wild populations inherently subject to the fundamental evolutionary processes; they do not consider domesticated populations, in which genetic change is dominated by decisions of breeders. The authors provide an overview of approaches that have been employed to elucidate adaptive evolution in natural populations in response to both geographical variation in climate in the past and to contemporary climate change. These approaches include observational studies conducted across spatial and temporal gradients, experimental manipulation of genetic and environmental factors, prediction of future evolution based on standing levels of genetic variation and selection gradients, and simulation modeling of evolutionary change.
Overview of Evolutionary Genetics Populations are constantly changing. An increasing number of studies have documented changes in natural populations, even over a few generations (Grant and Grant, 1993; Reznick et al., 1995; Bradshaw and Holzapfel, 2001; Re´ale et al., 2003; Franks et al., 2007). However, it is important to recognize that not all changes that have been observed in recent decades (e.g., Walther et al., 2002) in natural populations reflect evolutionary responses to natural selection. A clear distinction needs to be made between ‘‘environmental response’’ and ‘‘evolutionary response.’’
Environmental versus Evolutionary Response Environmental response of organismal traits, or phenotypic plasticity, reflects the direct dependence of organisms’ physiology, growth, development, and behavior on the environmental conditions they experience through their lifetimes (Bradshaw, 1965). Plastic responses do not involve changes in
the genetic composition of a population but manifest environmental influences on the expression of genes (e.g., flowering time, Aikawa et al., 2010). In contrast, evolutionary change is the change over generations in the genetic composition of a population. All populations are continually subject to evolutionary change. It results from several processes, including natural selection, i.e., variation among genotypes in survival or reproductive success. Natural selection is the basis for adaptation. Genotypes that express adaptive phenotypes make a greater genetic contribution to the subsequent generation; in this way, alleles that confer higher fitness in a given generation gain in frequency in the population. Natural selection may also favor plasticity that maintains high fitness in a variable environment. For example, a genotype that produces thin leaves in mesic conditions but thicker leaves when it develops in more arid conditions may have a survival or reproductive advantage over genotypes that do not respond in this way. If there is variation among genotypes in their phenotypic plasticity and this variation is under selection, plasticity itself can evolve (Via, 1993). In the context of climate change, phenotypic changes such as timing of flowering and breeding that correspond statistically with recent climatic trends are well documented (Parmesan and Yohe, 2003). Observation of such changes does not reveal the basis of these responses, whether plasticity in response to immediate environmental condition, adaptive evolution in response to selection mediated by environmental change, or a combination of these. Phenotypic plasticity may buffer populations against natural selection in the short term. However, the limits of phenotypic plasticity in maintaining fitness over a range of environments are poorly understood, and, over the long term, ongoing climate change is expected to exceed those limits (DeWitt et al., 1998). Thus, as climate continues to change, it is likely that natural selection will alter plasticity of traits as well as their expression in particular environments, given climate model predictions that include both directional change and increased variability.
What is Natural Selection? Natural selection occurs when genotypes in a population differ in fitness, their contribution of progeny, and the genes they carry, to subsequent generations. Over generations, natural selection is expected to increase the average fitness of populations in the environments in which they undergo selection. This process of adaptive evolution proceeds over generations at a rate that depends on the severity of genetic selection, the genotypic variation in fitness. Climate conditions that are novel relative to previous ones at a particular location are likely to impose a typically strong directional selection on traits, such as rooting depth, that are related to survival in dry conditions. This would be expected even if climatic changes were smooth. However, the prediction that climate is becoming more erratic implies that bouts of intense selection in one direction (e.g., favoring greater drought tolerance) will be interspersed with weaker selection or even selection in the opposite direction. Evolutionary dynamics may be governed by such extreme selective events (Grant and Grant, 2002; Gutschick and BassiriRad, 2003).
Evolution in Response to Climate Change Evolutionary Rates
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relative fitness and traits (Price, 1970):
The rate of evolutionary response to selection depends on both genetic variation and environmental conditions and is most simply illustrated by the breeder’s equation (1). The expected amount of phenotypic change (R) in a single trait per generation in response to selection depends on the strength of selection on that trait as measured by the selection differential (S), a statistical measure of the association between fitness and trait values, and also on genetic variation for the trait as expressed by heritability (h2): R ¼ h2 S
½1
Heritability (h2) estimates the fraction of the total phenotypic variance (VP) due to additive genetic variance (VA): h2 ¼ VA =VP
½2
VA is the variance in a trait that is attributable to segregation of alleles at all the genes that influence that trait, and the resemblance of relatives due to sharing of alleles at all these genes is proportional to h2 (Falconer and MacKay, 1996). VA, VP, and S are not static quantities. The expression of additive genetic variance and the total phenotypic variance depend on the immediate environmental conditions, as does the selection differential. Thus, estimates of heritability and selection are context dependent and are applicable to prediction of selection only in the specific environment for which they have been estimated. The single-trait breeder’s equation is not adequate to describe response to selection when multiple traits are under selection and are genetically correlated with each other. Genetic covariance between pairs of traits, each subject to selection, can promote the response of each to selection, if, for example, the sign of the genetic covariance is positive and both traits are selected in the same direction. Conversely, a positive genetic covariance between traits impedes response of both traits to selection if higher values of one trait and lower values of the other are associated with higher fitness. The genetic variances of traits and the genetic covariances between pairs of traits depend on direct effects of environment on organisms and the traits they express; genetic variation in traits and fitness may be reduced (Hoffmann and Parsons, 1991) or enhanced (e.g., Shaw et al., 1995) in harsh environmental conditions. Genetic correlations between traits can be included in predictions of selection response using a multivariate extension of the breeder’s equation: Dz ¼ Gb
½3
where the predicted change in the means of a set of traits (expressed in a vector, Dz) across one generation depends on the additive genetic variance–covariance matrix (G) and the vector of selection gradients (b) (Lande, 1979). As in eqn [1], use of this expression to obtain predictions of selection response requires taking the product of two estimates, each of which has substantial statistical uncertainty due to sampling and measurement error. Thus, interpretation is not straightforward. Alternatively, the response to selection can be estimated directly as the additive genetic covariance between
Dz ¼ CovA ½w,z
½4
where w is individual relative fitness (absolute fitness divided by mean fitness), and z is the vector of trait values (Shaw and Shaw, 1994; Etterson and Shaw, 2001; Hadfield et al., 2010).
What Processes Influence Genetic (co)variance? As with additive genetic variances, additive genetic covariances also depend on a population’s genetic composition, and strong selection over the extended period of climate change may radically deplete genetic variation. Spontaneous mutation steadily augments genetic variation; under changing conditions, novel mutations may more likely contribute to ongoing adaptation. Furthermore, influx of genes from genetically divergent populations increases genetic variation. Consequently, G (eqn [3]), which governs the immediate response to selection, i.e., from the current generation to the next, is expected to change with ongoing climate change, though the net effect of all the processes that influence G is not readily predictable. In populations where climatic conditions become so severe that population size drops dramatically, genetic variation is expected to decline due to genetic drift. By this process of random sampling, genes that could contribute to adaptation can be lost (e.g., Weber and Diggins, 1990). Moreover, as populations decline in size, inbreeding increases, reducing fitness itself (i.e., inbreeding depression) further impairing populations’ capacity for increase. Inbreeding may also slow the response to selection (e.g., Shaw et al., 1998). Moreover, the number of new mutations in a population declines directly with the population’s size, with the consequence that particular mutations, for example, those that could support adaptation to changing climate, are less likely to arise. These considerations underscore the intimate connection between the demography of populations and changes in their genetic composition. Evolutionary theory before 1990 tended to ignore this connection, but such simplification is especially likely to mislead in circumstances when conditions are so severe that populations become small and are at risk of extirpation. In many cases, such populations are likely to die out. For others, immigration can play the important demographic role of increasing the size of a population, enhancing its chance of persisting, in addition to contributing to its genetic variation (Holt and Gomulkiewicz, 1997).
Evolution of Plasticity The tendency for natural selection to favor adaptive plastic responses will depend on the extent to which climate increases in variability. In the simplest case, if climates were to change monotonically (e.g., becoming progressively warmer or drier), then natural selection may favor adaptive evolution via fixed genetic changes that result, for example, in earlier breeding or greater thermal/drought tolerance. However, in the more realistic case in which climate variability increases (Alley et al., 2007), and hence variability in natural selection does also, then adaptation involving plasticity may enhance fitness
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across a range of environments. However, reversals in genotypic fitness, either within the lifetime of an organism or between generations, are expected to impede evolutionary increase in population mean fitness because genotypes with high fitness under both sets of conditions will be rare (Via and Lande, 1985; Gillespie and Turelli, 1989; Van Tienderen, 1991; Gomulkiewicz and Kirkpatrick, 1992; Gavrilets and Scheiner, 1993a, b). Adaptive plasticity is also less likely to evolve in a highly erratic and unpredictable climate marked by extreme events.
Approaches to Understanding Evolution in Response to Climate Change Adaptation to Climate in the Past Past evolution in response to climate is evidenced by the current adaptation of organisms to their home environments, encompassing climate, among many other aspects. A high degree of adaptation to an environment is reflected in high fitness (comprising individual survival and reproduction) that contributes to persistence of a population in that environment. This implies that, in previous generations, the population has undergone natural selection in those (or similar) conditions and, as a consequence, its genetic composition has changed, with increased frequency of genes conferring greater fitness than would otherwise be the case.
to genetic differentiation, phenotypic plasticity, or some combination of these can be ascertained through ‘‘common garden’’ experiments in which populations are sampled from an environmental gradient and reared in common conditions (e.g., Reinartz, 1984; Lacey, 1988). By subjecting the populations to the same environment, such experiments demonstrate that differences detected among them in morphology, physiology, and phenology, in the common garden setting, must be genetically based. Furthermore, if this differentiation is related to the gradient from which they were sampled, they will retain clinal patterns in a common environment (e.g., Etterson, 2004a). Clinal patterns that disappear in a common garden can be attributed to phenotypic plasticity (e.g., Maherali et al., 2002). Expanded forms of the common garden approach involve multiple growing locations, including reciprocal transplant studies (Clausen et al., 1940; Etterson, 2004a, b) and provenance trials (e.g., Rehfeldt et al., 1999). These experimental designs make possible comparisons of the relative adaptation of populations under different climatic conditions, and in relation to the climates at the locations from which the populations were drawn. Manipulation of some particular aspect of climate as an added experimental component of a common garden may yield yet stronger evidence of past adaptation to prevailing climatic conditions.
Observations Over Time Range Limits and Climate Variables The limits of species’ ranges commonly coincide with abrupt spatial gradients in climatic attributes, and the geographic extent of a species’ range can sometimes be predicted with high confidence from climate data taken in a subset of its range (Peterson et al., 1999). The geographic ranges of species have shifted during past periods of climate change and shifts in range are ongoing. Shifts of the range of species may be an important component of the biological response to climate change in the future. However, it is not clear that range shifts of populations will proceed at sufficient rates, such that they will be subject to similar climatic conditions as climate changes. For example, it is often suggested that severe fragmentation of contemporary habitat is likely to impede dispersal. Moreover, interactions within and between species may thwart establishment of a population in locations beyond the current range where climate has become suitable for it. Beyond the role of geographic shift in a species range, the evolution of range limits is expected, even in the absence of climate change (Kirkpatrick and Barton, 1997).
Geographic Variation among Populations within a Species Species that occur across environmental gradients frequently express clinal patterns in phenotype that may suggest underlying local adaptation. However, these patterns do not necessarily reflect genetic differentiation, but may result from phenotypic plasticity, which may or may not be adaptive. The extent to which clinal patterns in phenotype can be attributed
Evolutionary response to climate change has already been documented for a few wild organisms for which long-term studies of field populations have been conducted. For example, over the past 30 years mosquitoes that breed in pitcher plants in the eastern US have evolved different genetically based photoperiodic cues for breaking dormancy that correspond to increases in the length of the growing season in recent decades (Bradshaw and Holzapfel, 2006). In Australia, 20 years of temporal sampling of fruit fly populations has demonstrated latitudinal shifts of clinal variation of genetic traits (Umina et al., 2005). Rapid evolution of clinal variation has also been observed for several invasive species since the time of establishment (e.g., Huey et al., 2000). It has also been inferred that the timing of breeding has evolved in a population of red squirrels in Canada. In the last decade, spruce trees have been producing their cones progressively earlier (Re´ale et al., 2003), and this has exerted selection on the squirrel population resulting in earlier breeding. By tracing the inheritance of timing of breeding from parents to offspring for several generations, these researchers undertook to distinguish genetic change from phenotypic plasticity and ultimately attributed the observed changes to both. The authors note, however, that Hadfield et al. (2010) have called the conclusions of this and some other studies into question because the statistical methods used do not fully account for sampling variance. Given the difficulty in obtaining high-quality empirical data sets of this kind that are sufficiently large to allow robust methods of analysis, it is not surprising that there are few unequivocal examples of genetically based evolution in response to contemporary climate change (Gienapp et al., 2008).
Evolution in Response to Climate Change Resurrection Ecology In a few cases, direct demonstration of the nature of contemporary change in wild organisms has been possible because propagules (e.g., seeds in tundra soil or eggs in lake sediments) were recoverable or fortuitously available such that ancestors could be revived and compared side-by-side with their descendants (Bennington et al., 1991; Vavrek et al., 1991; Hairston et al., 1999; Kerfoot et al., 1999; Franks et al., 2007). This ‘‘resurrection approach’’ (Davis et al., 2005; Franks et al., 2008) has permitted phenotypic and genetic comparisons of populations representing different times. The work of Franks et al. (2007) illustrates this approach. They compared the date of first flower of plants that were revived from seeds stored in 1997 with that of plants grown from the seed of their descendants sampled in 2004 following an intervening drought. This comparison yielded estimates of rates of evolution and comparison with changes predicted from quantitative genetics theory.
Experimental Manipulation of Population Genetics Artificial selection involves experimental imposition of selection to answer questions about potential rates of evolutionary change. In practice, a researcher selects from a population individuals that express phenotypes of interest, for example, drought tolerance or earlier flowering. The selected individuals are interbred with the expectation that, if the trait is heritable, its phenotypic mean will differ in the offspring of the subsequent generation. From eqn [1] we can see that if the strength of selection (S) is experimentally determined and the response to selection (R) is observed, we can estimate the realized heritability (h2) of the trait of interest. An alternative approach is to expose a population to an environment (e.g., higher temperatures) in which genetic variation in fitness is expressed, such that natural selection proceeds (Bennett et al., 1992). Following several to many generations, fitness and other traits are compared between the selected and control populations to determine the extent of evolutionary change. Experimental evolution by either of these approaches may demonstrate evolutionary change in numerous traits. Information obtained from studies of experimental evolution has improved our understanding of biotic response to climate change in numerous ways. For example, artificial selection studies have shown that it is possible that shifts in flowering time in herbaceous plant species that have been observed in nature (Parmesan and Yohe, 2003) may be due, in part, to evolutionary change (Burgess et al., 2007). In bacteria, studies where organisms evolved under experimental conditions have resulted in dramatic adaptive evolution in thermal tolerance (Lenski, 2001). It is particularly notable that adaptation proceeded in populations that initially lacked genetic variation; thus the adaptation that occurred depended entirely on newly arising mutations, and proceeded even under conditions of fluctuating selection. Mongold et al. (1999) have further shown that genes that can support adaptation beyond the presumed lethal thermal limit of E. coli fail to increase in frequency in competitive conditions. Consequently, only when populations decline in abundance does
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adaptation to such extreme thermal conditions proceed, a clear example of the intimate connection between demographic and genetic change. In contrast to the previous examples, some experiments to evaluate potential for adaptive evolution in response to aspects of global change have detected only limited evolutionary responses. Potvin and Tousignant (1996) manipulated both temperature and CO2 concentration and found that responses of wild mustard following seven generations in those conditions were primarily through nonadaptive plasticity. In summary, experimental evolution is a powerful approach that will continue to elucidate the rate of evolutionary change, the presence of genetic variation for traits that are under selection, and the role of genetic correlations in evolutionary change.
Prediction of Future Evolutionary Trajectories To predict adaptation in response to climate change, we need estimates for three fundamental pieces of information: the strength and direction of selection in future climates, the genetic variances of traits that are under selection in altered environments, and the extent to which these traits are genetically correlated with other traits. Selection regimes currently impinging on populations at lower elevation or latitude may simply shift to higher elevations or latitudes as climate warms and the geographical ranges of species track these shifts. However, populations may change in more complex ways because the ecological context, both abiotic and biotic, will be altered. Paleoecologists, having extensively studied assemblages of species in the past via the pollen record, have frequently noted that these assemblages often do not have present-day analogs, which suggests that environmental conditions are not closely replicated in different eras. A direct way to assess trends in selection is to do phenotypic selection analyses on data collected from longterm studies of field populations. However, data sets that are complete enough to document such temporal changes in selection on wild populations are rare (but see Grant and Grant, 1995). An alternative approach is to compare natural selection in current environments to selection in experimental conditions similar to those predicted for the future. However, most studies that have manipulated environmental conditions, such as temperature, precipitation, and CO2 have focused on changes in species composition rather than on patterns of natural selection, although there are a few exceptions (Totland, 1999). Insight into temporal changes in selection may also be obtained by characterizing changes in selection along environmental gradients that encompass a range of conditions similar to those predicted for a given location in the future (i.e., a chronosequence, Etterson, 2004a). This approach may provide an incomplete picture of future selection because native species composition will also be altered by climate change and invasive species, pests, and diseases may invade new territories and alter patterns of selection. Furthermore, patterns of selection may be more erratic in the future if climates become more prone to extreme events such as drought, heavy precipitation, heat waves, and intense tropical cyclones (Alley et al., 2007).
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Evolution in Response to Climate Change
Theory for Evolutionary Response to Changing Environment The persistence of populations in changing environments depends on both evolution and demography. Theory that couples evolutionary and demographic dynamics of closed populations has shown that even if adaptive responses are possible, densities may fall below some critical level such that populations are susceptible to extinction by stochastic processes (Bu¨rger and Lynch, 1995; Gomulkiewicz and Holt, 1995). Genetic variation in a trait subject to changing selection as environment changes can enhance the persistence of populations in a changing environment whether the population shifts in its range in conjunction with the changing environment (Pease et al., 1989) or not (Bu¨rger and Lynch, 1995). Levels of genetic variation and therefore, the potential for adaptive evolution, are not likely to be uniform among populations across the species range (Antonovics, 1976; Lenormand, 2002). As populations become increasingly fragmented, with reduced dispersal among subpopulations, their potential for local adaptation is expected to increase (Dickinson and Antonovics, 1973; Garcia-Ramos and Kirkpatrick, 1997). Nevertheless, even if marginal populations are not swamped by gene flow from central populations, adaptive evolution may be slowed due to strong selection causing genetic variance to be depleted (Fisher, 1930). Genetic drift may also erode genetic diversity, especially in small and isolated populations near the periphery of the species range or in remnant populations (Wright, 1931; Nei, 1973). Thus, fitness may be positively or negatively influenced by gene flow between populations. Adaptation may be more rapid with gene flow, both because it increases genetic variation in traits subject to selection (Swindell and Bouzat, 2006) and because it impedes genetic drift (Lopez et al., 2009), even in an environment that is constant through time. In populations spanning gradual environmental gradients, gene flow between adjacent populations is not expected to inhibit local adaptation because populations are similarly adapted. Marginal populations evolve in response to extreme conditions expanding their tolerance limits and geographic ranges. However, if the environmental gradient is steep, the process of local adaptation is swamped by gene flow between populations that are adapted to substantially different environments (Kirkpatrick and Barton, 1997).
Summary Evolution proceeds unceasingly in all biological populations. Rapid adaptation to human-mediated environmental change was evident long before climate warming became apparent. Consequently, there is no doubt that natural populations will continue to evolve and, in particular, that adaptation to changing climate is possible, in principle. However, it remains unclear how the several evolutionary processes – natural selection, mutation, gene flow, and genetic drift – will jointly alter any single population or the biota collectively. Even though natural selection is likely to proceed, there is insufficient understanding to predict for how many species and which species the rate and extent of adaptation will be
adequate to support persistence, given the very high rates of environmental change expected. Such predictions will require further empirical investigation (experimental, as well as observational) of genetic variation and natural selection, directly accounting for increasing variability of climate. Moreover, the remaining evolutionary processes and their interplay, all of which are sensitive to demographic aspects of populations, are expected to bear importantly on genetic change in nature. Research that accounts for these processes, as well as natural selection, will yield more reliable prediction of evolution and species persistence in the face of changing climate.
See also: Climate Change and Extinctions. Climate Change and Wild Species. Plant Phenology Changes and Climate Change
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