Evolutionary consequences of climate change

CHAPTER 2

Evolutionary consequences of climate change Susana M. Wadgymar*, Rachel MacTavish†, Jill T. Anderson† *

Biology Department, Davidson College, Davidson, NC, United States Odum School of Ecology and Department of Genetics, University of Georgia, Athens, GA, United States

†

Contents Evolutionary responses to climatic changes Climatic agents and phenotypic targets of selection Local maladaptation under climate change Migration and range shifts Phenotypic plasticity could buffer populations from decline Adaptive evolution Gene flow could facilitate adaptive evolution Global variation in evolutionary potential Species interactions and coevolution Incorporating species interactions into our understanding of evolutionary responses to climate change Belowground interactions Summary References Further reading

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Evolutionary responses to climatic changes Climatic agents and phenotypic targets of selection Natural populations are encountering novel environments as anthropogenic changes continue to increase in frequency and magnitude. In temperate and polar regions, climate change projections predict that many regions will experience a warmer and drier climate year-round (Fig. 1). Climate change will differentially influence the duration and timing of each season. In temperate regions, spring already starts earlier, and fall starts later, resulting in longer summers and shorter winters. In high-elevation and high-latitude regions, the earlier snowmelt and later snowfall expected in the spring

Ecosystem Consequences of Soil Warming https://doi.org/10.1016/B978-0-12-813493-1.00003-X

© 2019 Elsevier Inc. All rights reserved.

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Warmer and drier

Projected Contemporary Historic

Future precipitation Biological consequence

Longer summers Shorter winters

Spring

Summer

Autumn

Winter

Earlier snowmelt

Less rainfall

Later snowfall

Less snow

Frost Drought susceptibility stress

Spring

Frost Insufficient susceptibility winter chilling

Fig. 1 A depiction of the projected influence of climate change on season length, temperature, and precipitation, and the potential associated biological consequences of such an influence.

and fall, respectively, leave plants and soil-dwelling organisms susceptible to frost damage because they will not be protected by the thermal insulation provided by snow while air temperatures fluctuate between thawing and freezing conditions (Inouye, 2008). Depressed snowfall in the winter in concert with increased temperatures and reduced rainfall in the growing season will leave many organisms prone to drought stress (Stewart et al., 2005; Knowles et al., 2006; Rangwala et al., 2012; IPCC, 2014). Additionally, at low to mid latitudes, shorter winters may result in insufficient winter chilling, which could cause plants to remain dormant and fail to reproduce in the spring and summer (Zhang et al., 2007; Luedeling et al., 2009, 2011). In comparison to temperate and polar regions, aseasonal tropical regions have historically experienced minimal changes in temperature and photoperiod throughout the year, although seasonal tropical forests have regular and pronounced rainy seasons. Organisms inhabiting lower latitudes have evolved to commence life history transitions in response to subtle seasonal cues or to dependable precipitation events. The reliance of growth and development on historically predictable environmental conditions suggests that climate

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change could have similar potentially disastrous effects on natural tropical populations. Climate change will likely exert novel patterns of selection on natural populations worldwide and may become a predominant driver of evolutionary change in many systems. Thus far, few empirical studies have directly estimated selection under projected future climates (Davis and Shaw, 2001; Davis et al., 2005; Jump and Pen˜uelas, 2005; Jump et al., 2008; Shaw and Etterson, 2012; Franks et al., 2014). Abiotic and biotic environments shape adaptive landscapes, yet we know little about the specific causes of selection in most systems (Calsbeek and Cox, 2010; Sletvold et al., 2010; Kingsolver et al., 2012) or how agents of selection interact to influence the evolution of complex traits. Climate change is likely to favor the evolution of traits that promote stress tolerance or escape. For example, the evolution of higher thermal tolerance could reduce species’ vulnerability to climate change in regions projected to experience increases in temperature (Thompson et al., 2013). Similarly, behavioral changes can ameliorate the effects of climate change and permit organisms to maintain fitness (Kearney et al., 2009). In many reptile species, the sex of offspring is determined by the temperatures experienced during embryonic development ( Janzen, 1994). Rising temperatures may skew the sex ratios of taxa with temperature-dependent sex determination and may lead to population decline ( Janzen, 1994). Species can alter the temperatures of their nests or laying sites by nesting in a shaded location, digging deeper nests, or nesting during cooler portions of the season (Schwanz and Janzen, 2008; Telemeco et al., 2009). Climate-induced selection may also favor altered migratory patterns to better align with food resources (Pulido and Berthold, 2010), or shifts from specialization to generalization (Colles et al., 2009).

Local maladaptation under climate change Rapid shifts in abiotic conditions could disrupt long-standing patterns of local adaptation, instead favoring individuals from historically warmer and drier regions over local individuals (Wang et al., 2010; Aitken and Whitlock, 2013; Alberto et al., 2013; Franks et al., 2014; Wilczek et al., 2014; Anderson, 2016). Determining which aspects of the abiotic or biotic environment act as agents of selection and promote adaptive evolution requires manipulative experiments conducted in field settings. In a review of the local adaptation literature, Wadgymar et al. (2017b) found only four studies that identified the agents of selection that contribute to local adaptation in natural

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populations. In a metaanalysis of experiments that simulated future climates, Anderson (2016) found that climate change could depress viability and fecundity in native plant populations. Indeed, climate change may have already produced maladaptation in some systems. A reciprocal transplant of the annual plant Arabidopsis thaliana across four sites spanning the range of the species revealed that genotypes from historically warmer locales exhibited higher fitness than native genotypes in all cases (Wilczek et al., 2014). Similarly, populations of lodgepole pine (Pinus contorta) from sites experiencing high mean annual temperatures exhibited higher productivity than local populations at a site in British Columbia (Wang et al., 2006, 2010). Reciprocal transplants of white spruce, Picea glauca, demonstrated that populations are maladapted to current soil moisture conditions, and simulations suggest that the influence of future precipitation regimes on this adaptive lag will depend on corresponding shifts in temperature (Andalo et al., 2005). Local maladaptation could increase the risk of local extinction by reducing population sizes and depressing standing genetic variation within populations.

Migration and range shifts Most species are distributed across climatic gradients, often with populations arrayed along aridity gradients across longitudes or temperature gradients associated with elevational or latitudinal variation. As the climate changes, numerous species are shifting their distributions poleward and upslope in elevation (Parmesan and Yohe, 2003). Indeed, in one of the first studies of biological responses to climate change, Parmesan (1996) observed that the distribution of Edith’s checkerspot butterfly (Euphydryas editha) had already shifted 2° north in latitude and that high-elevation populations had greater persistence than low-elevation populations. For this study, Parmesan (1996) revisited locations with historical records of this species and extensively recensused the populations from 1992 and 1996. Prior to this work, the physical consequences of climate change were becoming apparent, but it was unclear whether natural communities were responding. Since that time, researchers have repeatedly demonstrated similar distributional shifts across a diversity of taxonomic groups (e.g., Parmesan et al., 1999; Beaugrand et al., 2002; Lenoir et al., 2008; Perry et al., 2005; Hickling et al., 2006;but see Zhu et al., 2012). Species with narrow geographic distributions are clearly at greater risk of extinction than those with broad ranges (Williams et al., 2007; Williams and Jackson, 2007). However, even those with broad distributions may experience reductions in population

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growth rates and local extinctions, with population contractions at the warmer edge of the range and potential expansions into historically cooler locations. For example, in South America, Duque et al. (2015) documented consistent compositional changes in plant communities, demonstrating that species from historically hotter locations (lowlands) are replacing upslope species in historically cooler locations across the Andes. That is, Colombian trees are migrating upslope from lowland into montane tropical forests at a rate of 2 (adults) to 5 (juveniles) meters per year (Duque et al., 2015), and this pattern is quantitatively consistent with upslope migration of tropical trees in Costa Rica and the Peruvian Andes (Feeley et al., 2011, 2013). These shifts in geographic distributions are primarily due to range contractions at the trailing (warmer) edge, rather than expansions at the leading (cooler) edge (Duque et al., 2015). Furthermore, these migration rates were typically slower than the rate of climate change in these regions (Feeley et al., 2011, 2013; Duque et al., 2015), begging the question of whether these neotropical forests will be able to keep pace with global warming. Extensive local adaptation may further hinder the ability of populations to adapt or migrate in response to rapid climate change as altered climatic conditions will likely depress population growth rates by reducing establishment, survival, and reproductive success (Anderson, 2016). Generalist species with extensive dispersal may have the greatest capacity to migrate and evolve under climate change (Berthouly-Salazar et al., 2013); however, it is challenging to predict migratory potential based on species’ traits (Angert et al., 2011).

Phenotypic plasticity could buffer populations from decline Climate-mediated selection may act directly on functional traits, or may instead favor increased phenotypic plasticity (Gienapp et al., 2014). Phenotypic plasticity is the ability of a specific genotype to produce variable phenotypes in different environments (Pigliucci, 2005). These changes in phenotype can be adaptive if organisms gain a fitness advantage in their altered form, contributing to population persistence or establishment (Yeh and Price, 2004). Alternatively, plasticity can be neutral if fitness is not affected or even maladaptive if fitness decreases (Ghalambor et al., 2007). In contemporary landscapes, plasticity can buffer populations against the immediate effects of climate change by maintaining or enhancing fitness, permitting species more time for evolutionary responses (Nicotra et al., 2010; but see Duputi
e et al., 2015). After environmental change induces

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a plastic response, subsequent selection could result in genetic assimilation, where altered phenotypes are canalized and permanently expressed (Waddington, 1952). Lastly, phenotypic plasticity itself has a genetic basis and can be targeted by selection (Baythavong and Stanton, 2010; Baythavong, 2011). For example, climate change has produced a mismatch between the timing of the breeding period for a Dutch population of great tits (Parus major) and their caterpillar prey (Visser et al., 1998). Nussey et al. (2005) show that plasticity in the timing of reproduction in great tits is heritable and has been increasingly favored by selection as spring temperatures increase with climate change. The authors postulate that plasticity in reproductive phenology could alleviate the degree of phenological mismatch between great tits and their primary food source, allowing them to withstand ongoing climate change. Variation in phenotypic plasticity within and among populations likely generates complex evolutionary responses to climate change. Whitlock (1996) describes how plastic genotypes, populations, or species will evolve more slowly than those with lower levels of plasticity. For species with extensive phenotypic plasticity or broad niche breadth, evolution in one environment will not increase fitness at the same rate as evolution in another environment if the genetic correlation of fitness across environments is less than one. Less plastic genotypes, or those with narrow niche breadth, can thus evolve higher mean fitness than more plastic genotypes when competing within the same niche, potentially leading to the competitive exclusion of the plastic genotypes in that environment. This occurs because specialist genotypes evolve in fewer habitats than do generalists and thus potentially experience stronger net selection across habitats. Furthermore, the strength of assortative mating may be higher between specialist genotypes because they occupy a narrower niche and are less reproductively isolated (Caillaud and Via, 2000; Hawthorne and Via, 2001). This leads to a comparatively faster fixation of beneficial alleles and a slower rate of accumulation of deleterious alleles when niche breadth is narrow (Whitlock, 1996). If changes due to plasticity are not great enough to increase the degree of assortative mating between plastic morphs, as it does for cichlid species (Meyer, 1987), the evolution of adaptive phenotypic plasticity may be limited. Plasticity may facilitate rapid evolutionary change if it leads to an increase in phenotypic or fitness variation in a population. Paenke et al. (2007) propose a method for determining how plasticity will affect the rate of evolution under directional selection. Their modeling approach suggests

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that plasticity will accelerate evolution when previously fit genotypes gain proportionately more fitness due to plasticity than do previously less-fit genotypes. In this case, the selection differential is greater, leading to faster evolution. If the opposite occurs, where previously less-fit genotypes gain proportionately more fitness from plasticity than previously more-fit genotypes, the differences in fitness between genotypes is reduced and selection becomes weaker. If thought of in the framework of the adaptive landscape, this prediction makes inherent sense. Plasticity must shift the population to a portion of the landscape with a steeper slope for evolution to be accelerated.

Adaptive evolution Climate change will likely impose strong novel selection on natural populations; the question remains whether populations have sufficient genetic variation to adapt to these altered conditions ( Jump and Penuelas, 2005; Franks and Hoffmann, 2012). Adaptive evolution depends upon the existence of genetic variation in functional traits as well as the strength of selection on those traits. Consequently, evolutionary biologists have long been interested in processes that maintain genetic variation in natural populations, including balancing selection and mutation-selection balance (Mitchell-Olds et al., 2007). The amount of genetic variation in a population is influenced by a variety of factors. For instance, levels of genetic variation are dependent upon patterns of assortative mating, or the degree to which mating patterns are nonrandom within or among populations. At one extreme, inbreeding arises when individuals with similar genotypes are most likely to mate with each other, resulting in reduced genetic variation (Charlesworth, 2003). In flowering plants, individuals with similar flowering schedules have greater opportunities for pollen exchange than individuals with contrasting flowering schedules (Weis and Kossler, 2004). In contrast, outcrossing can increase levels of genetic variation. For example, in heterostylous plants, morphs can only successfully mate nonassortatively (e.g., long-styled flowers mate with short-styled flowers) (Barrett, 1992). A species’ mating system can also determine the degree of genetic variation in a population, with species that reproduce via outcrossing harboring greater genetic variation than species that self-fertilize (Wright et al., 2013). Stochastic fluctuations in the numbers or frequencies of alleles in a population, or genetic drift, can randomly decrease genetic variation over time. However, smaller populations are more susceptible to drift and are thus

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more likely to suffer a decline in genetic variation (Ellstrand and Elam, 1993). Spatial or temporal variation in natural selection can maintain genetic variation in populations arrayed across environmental gradients (Estes and Arnold, 2007; Anderson et al., 2011; Wadgymar et al., 2017a). As we detail below, gene flow can also expand or erode the amount of genetic variation in a population. Combined with population size and demography, these factors likely interact to govern a population’s potential for adaptive evolutionary responses to selection (Morris et al., 2008; Bijlsma and Loeschcke, 2012; Gossmann et al., 2012). The rapid pace of contemporary changes in climate necessitate an understanding of other factors that constrain adaptive evolution. If novel selection drives genetically correlated traits in antagonistic directions, the evolutionary response could be negligible or even maladaptive, as seen in the annual legume Chamaecrista fasciculata (Etterson and Shaw, 2001). However, if selection is strong and demographic stochasticity minimal, evolution can proceed rapidly in response to environmental change (e.g., Franks et al., 2007; Thompson et al., 2013; Carlson et al., 2014). For example, Brassica rapa evolved novel flowering phenology that enables escape from drought after just 7 years of prolonged drought (Franks et al., 2007, 2016; Hamann et al., 2018). Similarly, Mediterranean wild thyme (Thymus vulgaris) has evolved reduced frost tolerance since the 1970s owing to relaxed selection occurring during warming winters (Thompson et al., 2013). Some species may face developmental or physiological limitations for responding to climate change. Species that rely on precise combinations or sequences of environmental cues for life history transitions may face additional challenges if climate change disproportionately disrupts distinct aspects of the environment. Wadgymar et al. (2018) demonstrated that the onset of flowering has advanced to earlier in the year for several plant species in a subalpine meadow. Experimental snow removal treatments confirm that early snowmelt and reduced snowpack are driving these shifts in phenology and reduce the proportion of plants that come in to flower. Furthermore, they show that phenological shifts expose some species to novel combinations of temperature and photoperiod, which could constrain future responses to continuing environmental change. Altogether, even when containing sufficient genetic variation in fitnessrelated traits to respond to natural selection, a population’s capacity for adaptive evolution may be limited by its genetic architecture or strict environmental dependencies.

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We can begin to elucidate the evolutionary responses of species to climate change using historical records, archived specimens or genetic material, and well-designed experiments. Long-term observational records are invaluable for gauging ecological responses to climate change, although it is impossible to distinguish between genetic and plastic phenotypic change without monitoring the survival and reproduction of individuals through time. For species that lack long-term trait-based or demographic data, museum and herbarium records can inform studies of trait variation and distribution through time (Parmesan, 1996; Primack et al., 2004; Elith and Leathwick, 2007). Additionally, genetic and plastic trait changes can be disentangled by comparing historical and contemporary populations of species using seed and egg banks ( Jankowski and Straile, 2003; Etterson et al., 2016). In other cases, climatic conditions can be controlled experimentally to either simulate past climates (Becklin et al., 2016) or future climates (Arnolds et al., 2015). Experiments conducted in nature are the most direct and informative way to gauge the patterns of natural selection imposed by climate change and whether populations can respond via adaptive plasticity or evolution. As we have stressed, limited genetic variation could restrict adaptive responses to climate change. In contemporary landscapes, multiple anthropogenic stressors are interacting to influence the eco-evolutionary potential of natural populations (Brook et al., 2008). Pollen records show clear patterns of migration in response to the retreat of the Pleiostocene glaciers (Davis and Shaw, 2001; but see McLachlan et al., 2005; Anderson et al., 2006), yet species then were not constrained by pervasive habitat fragmentation as they are now (Barnosky et al., 2012). Human land use not only restricts potential migratory routes, but it also dramatically reduces population sizes and connectivity among populations, and exposes natural populations to novel communities, invasive species, and altered abiotic conditions (Young et al., 1996; Damschen et al., 2006; Uriarte et al., 2010). Edge effects along habitat fragments can be pervasive, interfering with environmental conditions for tens to hundreds of meters into the interior of a patch (Holway, 2005; Laurance et al., 2011). Thus, habitat fragmentation can change the local selective regime, and depress rates of gene flow. In addition, by reducing population sizes, fragmentation diminishes within population genetic variation. All of these factors will reduce the ability of species to keep pace with climate change through adaptation and migration. Nevertheless, biodiversity threats from habitat loss and fragmentation, urbanization, overexploitation, invasive species, emerging diseases and other

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natural enemies, and climate change are typically considered in isolation. Studies that explicitly examine the evolutionary consequences of climate change in fragmented populations will go a long way toward generating more reliable predictions about the adaptive potential of natural populations under the novel selective regimes of climate change.

Gene flow could facilitate adaptive evolution In heterogeneous landscapes, gene flow can serve two key evolutionary roles: constraining and creative (Lenormand, 2002). For one, gene flow may limit adaptive population divergence by continuously introducing maladaptive alleles into local populations (Lenormand, 2002). Large populations in favorable environments typically have greater growth rates (λ) and produce more emigrants than populations in marginal habitats or those at the edges of the range. Asymmetrical gene flow from central to marginal populations can maintain positive population growth rates (Angert, 2009), thereby preventing local extinctions, but it can also prevent those populations from adapting to local conditions (Anderson and Geber, 2010). Gene flow among populations can also spread advantageous alleles, increasing the genetic variation upon which selection can act. Persistent strong directional selection—as expected under climate change—can deplete genetic variation from local populations (Buckley and Bridle, 2014). Gene flow could hasten adaptation to rapidly changing environments by introducing alleles that confer tolerance to stresses that are becoming more frequent and severe under climate change (Aitken and Whitlock, 2013). That is, gene flow could promote adaptation to novel suites of environments if alleles adapted to elevated temperatures, drought, reduced snowpack, or other conditions associated with climate change become introgressed into locally adapted populations in upslope or poleward locations (Aitken and Whitlock, 2013). This “evolutionary rescue” has been incorporated in to assisted gene flow conservation management plans, whereby individuals or genetic material from robust populations are introduced to imperiled populations to facilitate rapid evolutionary responses to selection (Aitken and Whitlock, 2013). Range expansions and migration are clear signals that natural populations are responding rapidly to climate change (Parmesan et al., 1999; Parmesan and Yohe, 2003; Hickling et al., 2006; Parmesan, 2006). Nevertheless, we know little about the importance of gene flow for promoting or constraining evolutionary responses to climate change (Kremer et al., 2012, 2014).

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Within a species, populations likely differ in their potential to adapt to ongoing changes (Hampe and Petit, 2005). For example, contracting populations at the trailing edge of the range of a species are less likely to adapt for several reasons. For one, these populations are located at the warmest edge of the distribution and will not experience an influx of migrants from equatorial or downslope populations. That is, these populations cannot be rescued by gene flow from populations that evolved in historically hotter sites (for a discussion of evolutionary rescue, see Alberto et al., 2013; Gonzalez et al., 2013). As conditions continue to change, novel selection could cause optimal trait values to fall far from current average trait values (Anderson et al., 2012), reducing average fitness and causing population growth rates to decline. For example, trailing edge populations of Scots pine (Pinus sylvestris) show reduced seedling survival under elevated temperatures and novel precipitation regimes projected with climate change (Matias and Jump, 2014). Whereas southern pine populations will likely experience reduced recruitment under increased temperature and drought stress, recruitment may increase in northern populations (Matias and Jump, 2014). These results highlight that biological responses to climate change likely differ across the range, with trailing edge populations experiencing declines and leading edge populations potentially growing (Matias and Jump, 2014). Diminishing population sizes puts trailing populations at risk of increased mortality due to both demographic and environmental stochasticity (Keith et al., 2008). That is, trailing populations will likely confront the challenges that face small populations, including increased risk that intrinsic and extrinsic factors could hasten population decline. For example, small populations are subject to demographic stochasticity (random fluctuations in birth and death rates) and environmental stochasticity (variation in resources and natural enemies), reduced genetic diversity, increased rates of genetic drift, inbreeding depression, and Allee effects (reduced mating success) (Heschel and Paige, 1995; Hampe and Petit, 2005; Heschel et al., 2005; Bijlsma and Loeschcke, 2012; Gossmann et al., 2012). Reduced genetic diversity will restrict adaptive responses to novel selection imposed by climate change.

Global variation in evolutionary potential The climate is not changing uniformly across the globe (Garcia et al., 2014). Rather, some regions—particularly landmasses in high-latitude areas—are experiencing heightened rates of climate change relative to other areas

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(Garcia et al., 2014). A slightly different picture forms when researchers calculate the change in temperature and precipitation relative to historical variation in local climates. In that case, novel nonanalog climates are likely to emerge primarily in tropical and subtropical regions where interannual variability in temperature and precipitation is generally much lower than in higher latitude areas (Williams et al., 2007; Williams and Jackson, 2007; Garcia et al., 2014). Spatial patterns in the strength of selection imposed by climate change will vary not only according to which regions are projected to experience the most drastic changes in climate, but also by which regions already experience extreme conditions. For instance, polar regions are forecast to endure drastic changes in temperature in the 21st century (IPCC, 2014). Species occupying high latitudes are likely experiencing temperatures below their thermal optima (Fig. 2) (Deutsch et al., 2008; Pelini et al., 2009; Arau´jo et al., 2013). All else being equal, increasing temperatures may immediately enhance the performance of species occupying high-latitude regions (Deutsch et al., 2008; Arau´jo et al., 2013). However, polar species may be negatively influenced by the indirect effects of rising temperatures. For example, plants may encounter an increase in the abundance or diversity of herbivores as the climate becomes warmer (Kurz et al., 2008; Currano et al., 2010; Liu et al., 2011; Mitton and Ferrenberg, 2012). Additionally, the nutritional content of plant tissues decreases under elevated CO2 (DeLucia et al., 2008; Robinson et al., 2012), resulting in the increased consumption of plants by insects. As such, increased herbivore pressures in polar regions may necessitate the rapid evolution of resistance or tolerance to herbivory, and herbivore-mediated reductions in performance counteract the beneficial direct effects of temperature on growth and reproduction (Fig. 2). In contrast to polar regions, tropical areas are expected to encounter a comparatively smaller increase in temperatures. However, species at low latitudes are often specialized to a narrow temperature range and are already living near their thermal optima (Deutsch et al., 2008; Arau´jo et al., 2013; Kingsolver et al., 2013; Garcia et al., 2014), in which case physiological constraints may impede any evolutionary responses to climate change. Indeed, a survey of 48 Sceloporus lizard species conducted from 1975 to 2008 from 200 sites across Mexico showed that 12% of species had become locally extinct (Sinervo et al., 2010). Models attributed extinction probability with increasing maximum temperatures and revealed that extinction risk was highest in species already functioning at their maximum thermal

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Performance

Polar species Temperate species Tropical species Future performance

Temperature

Fig. 2 Hypothetical thermal performance curves for species occupying polar, temperate, and tropical regions. Arrows and stars depict how performance may shift with climate change in each region. For species residing in high latitudes, the direct influence of increasing temperatures on plant performance may oppose the indirect influence of climate-mediated increases in herbivore pressure. In contrast, species in tropical latitudes may already be adapted to high levels of herbivory, but could rapidly be pushed outside of their thermal tolerances by climate change. As a result, the persistence of polar, temperate, and tropical species will likely be constrained by different physiological restrictions and selective pressures under climate change.

physiological limit. In addition, unprecedented drought stress will likely act synergistically with elevated temperatures to threaten tropical species (Dai, 2013). Unlike species in polar regions, those occupying tropical latitudes may have evolved to cope with other phenomena expected to change with temperature, like increased herbivory in plants (Coley and Barone, 1996). Nevertheless, any reductions in performance may exacerbate the negative consequences of increased temperatures on tropical species. Very little is known about thermal tolerances in plants, as thermal performance curves are primarily quantified in animal systems. We hypothesize that the increased thermal tolerance breadth that high-latitude animal populations display will hold in plant systems as well. Future studies should be designed to quantify thermal tolerance more precisely in plants from tropical regions and use these data to forecast potential responses to climate change. Species occupying mid-latitude regions are predicted to face moderate increases in temperature (Fig. 2). In this way, mid-latitude species may not be limited by the same physiological restrictions or strength of selection as their tropical or polar counterparts, resulting in a comparatively reduced risk of decline with climate change (Deutsch et al., 2008; Tewksbury et al., 2008).

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The majority of research exploring biological responses to climate change has been conducted in mid-latitude regions (e.g., Amano et al., 2010; Alexander et al., 2015; Harte et al., 2015), inhibiting scientists from predicting global patterns of biological responses to climate change. Direct (e.g., temperature) and indirect (e.g., herbivory) facets of climate change may interact and impose unequal fitness costs to organisms located across broad geographic areas. To improve our ability to predict which species will be most vulnerable under climate change, scientists must explore the impacts of multiple biotic and abiotic stressors in understudied regions. Phenotypic plasticity may be adaptive in portions of the range subject to temporal variation in environmental conditions, and maladaptive or nonexistent where conditions are less variable (Valladares et al., 2014; Duputie et al., 2015). Temporal variation in climate increases from equatorial to poleward latitudes; this observation led to the prediction that thermal tolerances and plasticity should be greater at higher latitudes ( Janzen, 1967; Ghalambor et al., 2006). Indeed, this pattern holds for many species of ectotherms, and high-latitude species often inhabit locations with temperatures below their physiological tolerances, suggesting that these highlatitude species may thrive under warmer climates (Deutsch et al., 2008; Arau´jo et al., 2013). If population sizes begin to contract owing to depressed fitness from elevated temperatures, they will lose genetic diversity while simultaneously producing fewer emigrants (Clark et al., 2012; Anderson, 2016). Thus reductions in fitness owing to climate change could diminish the potential for these populations to keep pace with new conditions via adaptation or migration (Nabel et al., 2013; Anderson, 2016). Furthermore, migration and gene flow may not provide the demographic or evolutionary rescue in these low- and high-latitude regions that we might predict in mid-latitude systems. Researchers typically assume that climate change will particularly imperil species and populations inhabiting high-elevation or high-latitude ecosystems because they cannot migrate into a more suitable habitat. Indeed, current climates are likely to disappear from high-latitude regions and tropical mountains (Williams et al., 2007; Williams and Jackson, 2007). Endemic species and others with very narrow geographic ranges in these regions will likely face grave extinction risks (Williams et al., 2007; Urban, 2015). However, for species with broader distributions, migration and gene flow from lower elevation or lower latitude populations could forestall or prevent local extinctions at the tops of mountains or the highest latitudes. In contrast, climate change, in concert with other anthropogenic stressors, could devastate

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tropical ecosystems (Brook et al., 2008). For one, limited genetic variation in thermal tolerance traits could constrain adaptation to novel climates (Kellermann et al., 2009). If Rapoport’s rule holds and tropical species truly have smaller ranges than species from higher latitudes (Stevens, 1989), then there might not be as much potential for gene flow to spread alleles that confer tolerance to new climates in tropical regions. Furthermore, local populations cannot be sustained by immigration from populations that evolved in areas with historically hotter and drier conditions. A metaanalysis revealed a higher risk of extinctions from climate changemediated causes in tropical regions (especially South America and Australia/ New Zealand) than in more northerly regions (North America and Europe) (Urban, 2015). Tropical regions receive much less attention from researchers than do temperate areas; for example, Urban (2015) noted that approximately 60% of the predictions pertaining to extinctions from climate change were made for species from North America and Europe. Tropical regions are both cradles and museums of biodiversity, harboring hyperdiverse and unique ecosystems (H€ ulber et al., 2010). Nevertheless, our understanding of climate change responses appears to be biased toward less diverse temperate ecosystems (Cavaleri et al., 2015). A thorough understanding of the global ramifications of climate change will only come from increased funding and other resources dedicated to examining the adaptive and migratory potential of tropical species.

Species interactions and coevolution Incorporating species interactions into our understanding of evolutionary responses to climate change Species interactions are ubiquitous in nature and are important drivers of diversification and speciation. The ecological significance of species interactions spans across biological levels of organization, and can be fundamental determinants of species distributions, community composition, associations among trophic levels, and ecosystem function. Species interactions can be classified in to several broad categories according to their effect on the wellbeing of each interacting partner. In mutualisms, each species derives a benefit from the interaction via an exchange of resources, protection, shelter, or enhanced reproduction. Examples of mutualisms include the supply of nitrogen by soil microbes called rhizobia in exchange for shelter and carbon from the roots of legumes (Long, 1989) and the protection of acacia plants against herbivory by ants in exchange for food and shelter ( Janzen, 1966).

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Exploitative interactions, like predation, parasitism, and mimicry, benefit one species at the detriment of the other. Competitive interactions are mutually disadvantageous to participating species, although not necessarily equally so if there is asymmetry in competitive ability. Interactions can occur without a benefit or cost to either or both species. For instance, amensalism occurs when one species inflicts harm on another but is otherwise unaffected by the interaction itself. Blue-footed boobies (Sula nebouxii) will establish nesting sites inland to avoid attacks from adult Nazca boobies (Sula granti) on their nestlings, while Nazca boobies are unaffected by the presence of blue-footed boobies (Townsend et al., 2002). In contrast, commensalism benefits one species with a neutral effect on the other. Larvae midge Metriocnemus knabi residing within the tubes of carnivorous pitcher plants are unaffected by cohabitation with larvae of the mosquito Wyeomyia smithii, while mosquito growth increases with midge density (Heard, 1994). Species distributions are governed by both abiotic conditions and biotic interactions (Louthan et al., 2015). In the context of climate change, migratory dynamics are complicated by species interactions (Gilman et al., 2010; Brown and Vellend, 2014; Classen et al., 2015; Louthan et al., 2015; O’Hara et al., 2016). Interacting species with different dispersal mechanisms and potential will likely undergo geographic range shifts at variable rates, which could disrupt mutualisms as well as antagonisms (Gilman et al., 2010). Species that outpace their natural enemies and competitors could exhibit rapid population growth in their expanded ranges (McCarthy-Neumann and Ibanez, 2012). In contrast, species involved in specialized mutualisms may fail to establish in novel ranges if the partnering species has a slower migration potential (Stanton-Geddes and Anderson, 2011). Most species interact with multiple natural enemies and mutualists, and predictions of climate change responses rarely account for the diversity of interactions that occur within a community. The biological influences of climate change will perhaps be most apparent when examining changing dynamics among plants, diseases, and pests. In fact, in a review on the potential for climate change to induce a widespread increase in disease risk for plants, Garrett et al. (2006) stated that “… the adaptive potential of plant and pathogen populations may prove to be one of the most important predictors of the magnitude of climate change effects.” Indeed, disturbances by fire impacted just 2% of the area decimated by insect and pathogen outbreaks from 1989 to 1994 (Dale et al., 2001), and insect outbreaks are expected to spread and intensify with climate change (Logan et al., 2003; Dukes et al., 2009). Apart from outbreaks, overall rates

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of herbivory will also rise, as increasing CO2 will depress the nutritional quality of plant tissue (higher C:N ratios), causing herbivores to consume more (DeLucia et al., 2008; Robinson et al., 2012). Futhermore, increasing temperatures will likely augment feeding rates for ectothermic insect herbivores (e.g., Currano et al., 2010; Liu et al., 2011; Mitton and Ferrenberg, 2012) and even hasten generation times (Mitton and Ferrenberg, 2012). Rapid herbivore migrations in response to changing conditions could expose previously naı¨ve plant populations and species to novel herbivore pressures (e.g., Kurz et al., 2008). As plants are sessile, they are likely to strongly experience the negative consequences of climate change directly through altered environmental conditions and indirectly through the widespread outbreaks of pests and diseases. For this reason, plants have become prominent biological indicators of climate change. With such a high prevalence and broad influence of species interactions, it is not surprising that species with frequent and impactful interactions can reciprocally influence each other’s evolutionary trajectories. These coevolutionary dynamics can vary in form and specificity. For example, pairwise coevolution can develop when two interacting species act as agents of selection on each other. Effective preening by the feral pigeon Columba livia selects for smaller body size in feather lice of the order Phthiraptera, presumably because smaller lice are able to escape removal (Clayton et al., 1999). In turn, higher louse loads lead to reduced survival of pigeons, resulting in selection against bill deformities that impair preening efficiency (Clayton et al., 2005). At its most extreme, pairwise coevolving species will develop specialized, obligate dependencies on each other for survival and reproductive success, as with fig trees and their wasp pollinators (Anstett et al., 1997). In contrast to pairwise coevolution, diffuse coevolution can arise when lineages or assemblages of interacting species promote reciprocal evolutionary change on one another. The Carolina horsenettle, Solanum carolinense L. (Solanaceae), experiences direct selection for increased resistance to a community of fruit-, flower-, and leaf-feeding insects and selection for decreased resistance to a stem borer, resulting in an overall constraint on the plant’s evolution of resistance (Wise and Rausher, 2013). Most species reside within a diverse community with complex interaction networks, and thus likely participate in a fluid and intricate combination of pairwise and diffuse coevolutionary associations. Recently, researchers have begun to uncover the influence of intraspecific genetic variation on species interactions, where the form, symmetry, or frequency of the interaction between two or more species will vary among

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specific pairings of interacting genotypes. For instance, in an experiment designed to examine genotype-specific competition between two cooccurring species of goldenrod, Solidago altissima and Solidago gigantea (Asteraceae), Genung et al. (2012) discovered that genotype-by-genotype (G  G) interactions affected total pollinator visitation rates to S. altissima. A few studies have demonstrated that the effect of interactions between interspecific genotypes can be environmentally context dependent. In an investigation of genotypic interactions between barley and aphids, Tetard-Jones et al. (2007) showed that the reciprocal influence of genotype on plant height or aphid parthenogenetic reproductive success depended on the presence or absence of rhizosphere bacteria. Bryner and Rigling (2011) observed that growth and sporulation of the fungus causing chestnut blight (Cryphonectria parasitica) depended on the genotype of the hyperparasitic virus Cryphonectria hypovirus-1 that infected the fungus and the temperatures that they experienced. Similarly, the survival and growth of early life history stages in genotypes of the Pacific oyster Crassostrea gigas infected by specific genotypes of bacteria from the genus Vibrio are temperature-dependent (Wendling et al., 2017). These genotype-by-genotype-by-environment interactions (G  G  E) demonstrate that components of the abiotic and biotic environment can mediate genotypic interactions among species and suggest that environmental change may have important consequences for the coevolutionary fate of interacting species. Our ability to predict which species or populations will be particularly susceptible to decline with climate change may be improved by examining the effects of environmental change from a coevolutionary perspective. Northfield and Ives (2013) examined whether coevolutionary relationships can enhance or impede the response of populations to environmental change using a modeling approach. Their results suggest that the effects of climate change on coevolving species depends on whether the species involved have competing interests. Species have conflicting interests when an increase in the density of one species results in a decrease in the growth rate of the other species. Examples include predator-prey relationships, direct competition, or mutualisms where it is possible for one species to switch from being a cooperative partner to one who cheats or exploits. Species have nonconflicting interests when an increase or decrease in the density of one species results in a similar effect in the other. Species in most mutualisms fall within this category, as well as competing species who alter their behavior, phenology, or niche space to reduce interacting with their competitor. Simulations demonstrated that coevolution between species that have conflicting

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interests reduces the effects of climate change because of a negative feedback between coevolutionary and environmental effects. In contrast, a positive feedback between coevolutionary and environmental effects may result in an enhanced effect of climate change on species with nonconflicting interests. This model suggests that a species’ coevolutionary history can mediate its response to environmental change, and that species in mutualistic relationships may suffer the greatest risk of extinction with climate change. Most species engage in an intricate web of interactions with members of their community. If climate change influences species disproportionately, many currently stable species interactions may become imbalanced or expunged, leaving portions of the community-wide interactive network vulnerable to collapse. In this way, even species that are not directly impacted by climate change can be indirectly influenced via their interactions with affected species. Nearly all of the explorations of the influence of climate change on species interactions has focused on ecological phenomenon, while evolutionary studies are sorely lacking (Alexander et al., 2015).

Belowground interactions Empirical studies of eco-evolutionary responses to climate change generally focus on aboveground interactions among plants, their mutualists, and their antagonists in the context of elevated temperatures and shifted rainfall (Shaver et al., 2000). Equally important and understudied is the role of climate change on interactions among plants and soil microbes and their effects on ecosystem function (Classen et al., 2015). For instance, plant root traits can act as important drivers of carbon sequestration, soil stabilization, and nutrient cycling (Bardgett et al., 2014). Elevated soil temperatures increase carbon and mineral processing when plant roots and litter are present, thereby increasing heterotrophic microbial respiration and releasing carbon and nutrients into the atmosphere or bioavailable sediment pools (Suseela et al., 2012; Frey et al., 2013). Indeed, climate change may be augmented by the accelerated release of carbon dioxide caused by increased microbial respiration in thawing arctic and subarctic permafrost (Davidson and Janssens, 2006; Zimov et al., 2006; Koven et al., 2011). Nonetheless, the potential for belowground biotic processes to counteract or augment the effects of climate change on ecosystem processes should motivate studies that examine the influence of environmental change on species interactions and plant performance. For example, drought stress can influence the community structure of soil microbes and mediate the adaptation of plants to novel conditions

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(Classen et al., 2015). Lau and Lennon (2012) found that plants exhibited local adaptation when their associated microbial communities matched historical environments. In addition, in a subalpine meadow-warming experiment, drying soils limited microbial activity and shifted plant community composition and richness (Price and Waser, 2000). Our understanding of the consequences of climate change on ecosystem function would be expanded by further work on the synergistic or antagonistic effects of environmental conditions and species interactions on the abundance, survival, and reproductive success of plants. Soil mesofauna and macrofauna can profoundly influence soil characteristics, including infiltration rates, the mobility of nutrients, and the growth, metabolic activities, and abundances of bacterial and fungal species (Neher and Barbercheck, 1998). While soil mesofauna and macrofauna can influence the surrounding animal and plant communities and govern the stability of ecosystem processes, their sensitivity to climate change has only been examined in an ecological context. In an experimental manipulation of temperature and nutrient availability, Ruess et al. (1999) found that elevated temperatures and nutrient availability shifted the composition of nematode communities toward fungal- and plant-feeding species. Similarly, Bokhorst et al. (2012) detected a shift from small-bodied to large-bodied microarthropods after simulating a winter soil- and air-warming event in the subarctic heathlands. Ha˚gvar and Klanderud (2009) observed a comparable shift in microarthropod communities under temperature and nutrient manipulations, with rapid-growing species becoming more abundant and an overall reduction in species number. Future studies could uncover the consequences of climate change on local adaptation in soil fauna by directly measuring their survival and growth in artificial, contained populations or communities exposed to relevant climatic manipulations. To the best of our knowledge, the adaptive potential of soil microbes and viruses in natural systems has never been explored, leaving a high degree of uncertainty about whether climate change will elicit evolutionary responses in these organisms. The ecological responses of soil microorganisms to climate change have been studied in some systems. Castro et al. (2010) found that factorial manipulations of temperature, CO2, and precipitation interacted to differentially influence the overall abundance and composition of bacterial and fungal communities. Rinnan et al. (2007) discovered that soil microbial biomass in arctic heaths was unaffected by temperature, nutrient, and light manipulations until being exposed to approximately 15 years of sustained treatment. This time lag may reflect an indirect effect of these

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variables through their direct influence on community composition and plant biomass production. Barberan et al. (2014) found that genome size and genes associated with specific functional traits correlated with habitat breadth in soil bacteria sampled across a portion of Central Park in New York City, New York. This suggests that an exploration of genomic traits coupled with phylogenetic analyses may be an informative option for studying the impacts of climate change on organisms that cannot be phenotypically characterized. Microbial community composition and biodiversity in soils is linked to soil ecosystem functions including plant diversity, nutrient turnover, carbon sequestration; decreased microbial diversity or altered community composition can negatively affect ecosystem function (Wagg et al., 2014). These studies cumulatively demonstrate that interactions between multiple drivers of climate change can affect a diverse array of microorganisms and that demonstrates that taxonomic, functional, and eco-evolutionary explorations of microbial responses to environmental change are possible. The influence of climate change on microbes has largely been examined indirectly via the effects of microbial processes on macrofauna and flora or on ecosystem function. Pounds et al. (2006) linked the mass extinction of harlequin frog species of the genus Atelopus in the American tropics to the accelerated growth of a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) caused by changes in diurnal patterns of temperature. Pfender and Vollmer (1999) found that higher winter temperatures increased survival in overwintering rust fungi (Puccinia graminis), which increases instances of stem rust disease on perennial ryegrass and tall fescue. While ecologically impactful, it is unclear whether these and similar phenomenon are driven by evolutionary change, transitions in community composition or abundance, and/or shifts in distribution.

Summary Climate change has the potential to directly and indirectly influence the direction and rate of evolution in natural populations. Thus far, most examinations of biological responses to climate change have focused on ecological responses, or have examined evolutionary responses theoretically, using simulations, or by conducting experiments in controlled greenhouses and laboratories. Species partake in a complex suite of interactions with their abiotic and biotic environments. Future work should explore the collective influence of factors that could influence climate-mediated evolutionary

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trajectories, including the roles of phenotypic plasticity, gene flow, genetic constraints, and species interactions. Furthermore, to gain a comprehensive understanding of species’ responses to climate change, we must focus future research efforts in underexplored regions of the world, like the tropics, and on understudied taxa, including soil microorganisms.

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Further reading Sakalli, A., Cescatti, A., Dosio, A., G€ ucel, M.U., 2017. Impacts of 2°C global warming on primary production and soil carbon storage capacity at pan-European level. Climate Services 7, 64–77.