Introduction

Spatial and temporal heterogeneity in abiotic and biotic environmental conditions are ubiquitous. Across evolutionary time, organisms and populations have continually adapted to this heterogeneity. Natural selection stemming from local environmental conditions has favored those genetically determined phenotypes that are best adapted to prevailing conditions. For instance, in many geographically widespread species, populations from different latitudes and altitudes often show genetically based differentiation in their phenotypic appearance, physiology, and life history. Evolutionary biologists recognize such differentiation as local adaptations in the case where the local populations have a higher fitness than others when placed in this environment once other factors like inbreeding depression in populations are controlled (Kawecki & Ebert, 2004; Blanquart, Kaltz, Nuismer, & Gandon, 2013).

Once faced with changing environmental conditions—such as brought along by climate change—populations have basically three different means to respond. First, they can stay adapted by changing their genetic constitution through the process of evolution. Given that adaptation to local conditions is common, this is expected to occur regularly as long as sufficient time is available. Second, they can respond by phenotypic plasticity, which refers to genotypes’ ability to express different phenotypes depending on the prevailing environmental conditions. Third, a population facing maladaptation in the altered conditions may migrate or move to a different location where the conditions are similar to those preceding the environmental change.

There is no doubt that all three mechanisms are used by organisms and populations to stay adapted to their environments in the face of climate change. For instance, massive pole-ward range shifts in the distribution area of many organisms over the past few decades have been reported both from marine and terrestrial ecosystems (Walther et al., 2002; Perry, Low, Ellis, & Reynolds, 2005; Chen, Hill, Ohlemüller, Roy, & Thomas, 2011). Likewise, phenotypic plasticity as a way of responding to recent changes in climatic conditions appears to be widespread. For instance, many bird species seem to track changes in the spring phenology by advancing their migration and breeding schedules with the aid of phenotypic plasticity (Gienapp, Leimu, & Merilä, 2007; Charmantier & Gienapp, 2014). However, in contrast to range shifts and phenotypic plasticity, only genetically based evolutionary responses may provide an opportunity for populations to stay adapted in situ over extended periods of time. An important question is whether adaptation can occur quickly enough to have much impact on climate change adaptation.

Genetics of Climate Change Responses

In order to have evolutionary impact on organisms or populations, climate change must directly or indirectly influence a population’s genetic constitution (Figure 1).

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Figure 1. A schematic illustration of the paths through which climate change can influence likelihood and rate of evolutionary response. Thick green and red arrows refer to increase and decrease, respectively.

Direct genetic impacts refer to changes in allele frequencies and gene expression levels in one or more loci caused by changes in selection pressures, leading to increased adaptedness of a population. Indirect population-based genetic impacts refer to genetic changes caused by changes in those demographic properties (e.g., effective population size) of populations that influence their genetic constitution. These can be positive but also negative, such as when the expression of inbreeding depression is increased due to a sharp decrease in population size. Both kinds of genetic changes can be detected either by population genetics or by quantitative genetic methods.

Direct Genetic Effects

Changes in abiotic and biotic environmental conditions can affect the direction or strength of natural selection on organismal traits and lead to genetically based shifts in phenotypic distributions in populations. Such evolutionary responses have been documented in several studies (e.g., Bradshaw & Holzapfel, 2008; van Asch, Salis, Holleman, van Lith, & Visser, 2013). Some of the strongest evidence for such changes comes from shifts in the frequencies of discrete phenotypes that are under selection and have a known genetic basis. In this way, shifts in frequencies of melanism color phenotypes (Roulin, 2014) including color phenotypes in owls (Karell, Ahola, Karstinen, Valkama, & Brommer, 2011) have been linked to evolution under climate change.

However, the majority of adaptive shifts involve quantitative traits, and for these traits it has been harder to demonstrate genetically based shifts linked to climate change (Gienapp, Teplitsky, Alho, Mills, & Merilä, 2008; Merilä & Hendry, 2014) except in a few cases such as changes in the photoperiodic response of pitcher plant mosquitoes that allows the mosquitoes to take advantage of a longer favorable season at high latitudes (Bradshaw & Holzapfel, 2008). This partly reflects the difficulty in proving that an observed phenotypic change in the mean value of given trait in a given population is actually genetic, rather than representing a plastic response to changed environmental conditions.

Although the pioneering literature on evolutionary impacts of climate change (e.g., Holt, 1990; Hoffmann & Blows, 1993; Lynch & Lande, 1993) called explicitly for genetic evidence, much of the subsequent literature made inferences about evolutionary change based on purely phenotypic data. Because phenotypic and genetic responses do not necessarily align, but can even act in opposite directions (Conover & Schultz, 1995), evolutionary inference based on purely phenotypic data is not possible. A concrete example of this is provided by the study of red-billed gulls in New Zealand: while the body size of gulls has declined over time along warming ambient temperature, genetic analysis of this temporal cline shows that this change is unlikely to be genetically based (Teplitsky, Mills, Alho, Yarrall, & Merilä, 2008). This and similar findings from other studies (Gienapp et al., 2008) call into question evolutionary inference about climate change responses when genetic data is lacking. Unfortunately, this applies also to paleontological studies (e.g., Smith, Betancourt, & Brown, 1995) where acquisition of genetic evidence is often impossible.

Apart from the evidence for climate change–driven evolutionary changes coming from quantitative genetic approaches, evidence for direct impact of climate-mediated shifts in genetic constitution of populations can be obtained with the aid of population genetic methods (Hoffmann & Daborn, 2007). Studies made on Drosophila flies provide some of the best-known cases of climate change–mediated changes in genetic constitution of populations along latitudinal clines (Umina, Weeks, Kearney, McKechnie, & Hoffmann, 2005; Balanyá, Oller, Huey, Gilchrist, & Serra, 2006). Using genetic markers (allozyme allele frequencies or chromosomal inversion polymorphisms), these studies demonstrated that shifts in the frequency of particular alleles or chromosomal arrangements had taken place over two decadal periods parallel with shifts toward warming climate (Figure 2).

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Figure 2. Examples of climate change–associated genetic changes in two fruit fly species. A. Temporal shift in the allele frequency in alcohol dehydrogenase locus in Drosophila melanogaster over a latitudinal gradient in Australia over a two decadal period (redrawn from Umina et al., 2005). B. Temporal covariation in shifts in temperature and frequency of chromosomal inversion variants in 26 Drosophila subobscura populations from three different continents (redrawn from Balanyá et al., 2006).

Because the particular alleles (or chromosomal arrangements) showing temporal shifts were those associated with adaptation to warm environments based on findings from earlier studies, these findings provide compelling evidence for climate change–driven evolution. Changes in the frequencies of inversions may be particularly important in terms of climate change adaptation, because inverted regions lock up combinations of alleles across many loci. For instance, in Drosophila melanogaster many of the genes that vary along climate gradients appear to be located inside one inversion (Fabian et al., 2012). Similar evidence for climate change–mediated evolution has also become available from several other insect (Schilthuizen & Kellermann, 2014), fish (Crozier & Hutchings, 2014) and plant (Franks, Weber, & Aitken, 2014) studies. However, marker-based evidence is still rather rare, although the revolution in molecular biology brought along by new sequencing technologies provides new means to document and study evolutionary changes in the wild (e.g., Hoffmann & Daborn, 2007; Neale & Kremer, 2011). These methods, especially when applied to historical samples, may provide means to uncover footprints of climate change–associated genetic changes as illustrated by study of polar and brown bear genomes (Miller et al., 2012).

Genetic responses to selection mediated by climate change are possible only if the traits under selection are genetically variable. Although most traits and populations harbor abundant genetic variance in almost all traits studied, at least when measured under controlled conditions (e.g., Mousseau & Roff, 1987), there are also situations where lack of suitable genetic variation may be constraining evolutionary response to climate change–mediated selection. For instance, in a study of tropical Drosophila flies, a lack of genetic variability in desiccation tolerance would likely constrain the species adaptation to increasing aridity (Hoffmann, Hallas, Dean, & Schiffer, 2003). Similarly, lack of or very low additive genetic variance for thermal tolerance and breeding have been suggested to constrain climate change adaptation in the copepod Tigriopus californicus (Kelly et al., 2012) and the red-billed gull (Chroicocephalus novaehollandiae; Teplitsky, Mills, Yarall, & Merilä, 2010), respectively. These examples bring up another important consideration: the direct influence of environmental conditions on expression of genetic variability in traits under selection.

The amount of genetic variability in a trait and population is not constant, but levels of expressed variation may vary as the environmental conditions change. Consequently, by altering environmental conditions, climate change may directly impact upon the amount of genetic variation a trait is expressing, and thereby also its evolvability. Unfortunately, it is not possible to make generalizations as to whether unfavorable conditions generated by climate change are expected to increase or decrease expressed genetic variation: both outcomes are possible (Hoffmann & Merilä, 1999). Hence, whether these impacts would facilitate or constrain adaptation to climate change is not known. The increased interest toward studies quantifying effects of environmental conditions on expression of genetic variability after methods for simultaneous quantification of expression levels in thousands of genes have become available (Alvarez, Schrey, & Richards, 2015) may clarify this issue in the future.

The Role of Phenotypic Plasticity

An organism’s ability to adjust its phenotype in response to prevailing environmental conditions can be adaptive. For instance, when faced by changing climatic conditions, populations may adjust their phenology, physiology, or morphology to ensure that their reproductive period occurs at a time that environmental conditions are favorable. Evidence for phenotypically plastic changes on climate change is ubiquitous, and examples of this seem to exceed examples of genetically based evolutionary responses (Merilä & Hendry, 2014). While this may mean that phenotypic plasticity is a relatively more important means for populations and organisms to cope with climate change, one should keep in mind that it is far easier to detect plastic than genetic changes.

Although plastic responses are by definition nongenetic (in the sense that the change in phenotype is not caused by allelic shifts), the ability to express phenotypic plasticity may be genetically variable (Schlichting & Pigliucci, 1998). Hence, levels of phenotypic plasticity can also be selected and evolve. In fact, many conspicuous examples of phenotypic plasticity—such as induced predator defense structures in many animals (Tollrian & Harvell, 1999)—are likely to have evolved as adaptations to variable environments.

Plasticity and evolutionary genetic changes may not act independently, in that plasticity may facilitate evolutionary adaptation (e.g., West-Eberhard, 2003; Pfennig et al., 2010), including under climate change (Lande, 2009; Chevin, Lande, & Mace, 2010). There is evidence that some evolved differences among populations from different environmental conditions are similar to the plastic changes induced by the same environmental conditions. Hence, phenotypic plasticity may provide a stepping stone toward adaptation. Possible mechanisms allowing plastic responses to influence genetic adaptation include the Baldwin effect (Simpson, 1953) and genetic assimilation (Waddington, 1953; see also: Crispo, 2007). However, although theory suggests that these effects are potentially important in climate change responses (Lande, 2009; Chevin et al., 2010; see also: O’Dea, Noble, Johnson, Hesselson, & Nakagawa, 2016), empirical studies of such phenomena within the context of climate change are lacking.

Finally, whether or not plasticity is important for evolutionary adaptation in the long-term term, it is clear that the short-term benefits from plasticity for individual and population persistence can be large. This is nicely illustrated by results of an experimental study of sheepshead minnows (Cyprinodon variegatus) by Salinas and Munch (2012): the rate adaptation (sensu lato) to increased temperature had the potential to be ten times faster via trans-generational plasticity than through evolutionary (genetic) adaptation. Here, trans-generational plasticity refers to (environmental) maternal effects where environmental cues (in this case, high temperature) experienced by parents prior to fertilization triggered a modification of offspring phenotype (in this case, improved offspring growth performance) in response to high temperature. Transgenerational plasticity is widespread (Jablonka & Raz, 2009), and there is some evidence to suggest that it may provide important means to cope with a warming climate (e.g., Donelson, Munday, McCormick, & Pitcher, 2012; Parker et al., 2012; Shama et al., 2014). However transgenerational effects can also have negative consequences, as maternal exposure to stressful thermal conditions can decrease reproduction and survival of the offspring generation (see O’Dea et al., 2016 for further examples). Likewise, although phenotypic plasticity in general can be adaptive in “buying time” for a population subject to directional selection stemming from climate change, it may also be detrimental in reducing the effectiveness of natural selection toward genetic adaptation (Ghalambor, McKay, Carroll, & Reznick, 2007; Nunney, 2016). In fact, theoretical work suggests that this may be generally the case if the traits conferring adaptation to climate change are determined by many, rather than few, genetic loci (Nunney, 2016).

The Problem of Causality

While it is clear that climate change is likely to alter the direction and strength of natural selection acting on different traits and populations, ascribing temporal genetic shifts to selection mediated by climate change can be challenging. Unfortunately most studies of climate change evolution rely on correlational data; a shift in alleles or genetically based phenotypes is correlated to changes in ambient temperatures or some other variable. A genetically based shift could, however, also be responding to some unmeasured environmental factor correlated with a climatic trend.

This problem of assigning causality is not restricted to the study of evolutionary impacts of climate change alone, but it is of particular concern because many other environmental changes caused by humans (e.g., increasing pollution, habitat loss and degradation, changing rates of exploitation) covary with the warming trend. While there are ways to deal with this problem, none of them are entirely bulletproof (Merilä & Hendry, 2014). However, experimental evolution (Potvin & Tousignant, 1996; Lohbeck, Riebesell, & Reusch, 2012) and mesocosm (van Doorslaer, Stoks, Jeppesen, & De Meester, 2007) experiments in climate change context provide means to manipulate candidate drivers of observed responses and isolate the causal one from alternatives. Of course, such experiments are not possible in all systems, and the results of experimental manipulations may not reflect processes in wild populations. Nevertheless, well-replicated experimental studies conducted in climate change contexts may show that evolutionary responses to changes in parameters involved with ongoing climate change can take place, and lead to predictions as to what might be expected in wild populations.

Rate of Environmental Change

There are concerns that the rates of environmental changes caused by ongoing climate change are too fast to allow many organisms, especially large organisms with long generation times, to maintain adaptedness. Theoretical studies (Lynch & Lande, 1993; Bürger & Lynch, 1995) suggest that maximal sustainable rates of evolutionary change are on the order of 0.1 haldanes (i.e., phenotypic standard deviations per generation) or less, whereas the rates expected under current climate change projections will often require faster adaptation (e.g., Gienapp, Leimu, & Merilä, 2007). Hence, widespread maladaptation and extinctions are expected. These concerns are compounded by the expectation that the amount of genetic variation harbored by populations and available for selection will be reduced by habitat destruction and fragmentation caused by human activities. On the other hand even for species with long generation times, including trees, ongoing gene flow between populations adapted to different environments such as along a climatic gradient may help facilitate the persistence of species (Kuparinen, Savolainen, & Schurr, 2010). There is also good evidence from experimental studies that the introduction of new genetic material into small populations can increase standing genetic variation and decrease the risk of extinction (Hufbauer et al., 2015). Likewise, as discussed previously and shown in Chevin, Lande, and Mace, (2010), the current projections of maximum sustainable rates of evolutionary changes may be overly conservative if the contributions of phenotypic plasticity and genetic assimilation on climate change adaptation prove to be important.

Evolution as a Management Tool

The recognition that evolutionary adaptation may help populations to adapt to climate change at least in some situations has led to increasing interest in facilitating evolutionary adaptation. Enhanced rates of gene flow are seen as providing a way for economically important tree species to maintain adaptedness (Rehfeldt et al., 2014). Even where there is uncertainty about future climatic conditions, enhanced gene flow may provide an insurance policy particularly for plants where at least some genotypes can survive future conditions (Sgrò, Lowe, & Hoffmann, 2011). More radical solutions such as hybridization and genetic introductions across large geographical distances are being proposed as ways of improving adaptedness in organisms such as corals when persistence under future warming conditions seems unlikely (van Oppen, Oliver, Putnam, & Gates, 2015).

Conclusions

In conclusion, while evolutionary impacts of selection pressures generated by climate change are expected to be widespread and profound, these evolutionary impacts are not only hard to predict, but also extremely challenging to document. In contrast to ecological impacts of climate change, demonstrating evolutionary impacts requires evidence of changes in the genetic constitution of a given population. While such evidence is hard to come by, there are studies showing that such transformations are occurring, and more evidence for evolutionary responses to climate change will be uncovered with time. However, in the light of available evidence, it seems likely that the expected rates of environmental changes brought by climate change will often be too high for organisms with long generation times to track and stay adapted to changing conditions in situ unless they occur along sharp gradients where gene flow can result in a continual influx of adapted genotypes. Consequently, rather than seeing widespread adaptation to changing climatic conditions, the future may see evidence for range shifts, expirations, and extinctions as responses to climate change. This is especially likely in the case of organisms with relatively small population sizes and long generation times, and raises the issue of whether management strategies aimed at enhancing evolutionary resilience might be introduced in such circumstances.