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      Climate change, adaptation, and phenotypic plasticity: the problem and the evidence

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          Abstract

          Many studies have recorded phenotypic changes in natural populations and attributed them to climate change. However, controversy and uncertainty has arisen around three levels of inference in such studies. First, it has proven difficult to conclusively distinguish whether phenotypic changes are genetically based or the result of phenotypic plasticity. Second, whether or not the change is adaptive is usually assumed rather than tested. Third, inferences that climate change is the specific causal agent have rarely involved the testing – and exclusion – of other potential drivers. We here review the various ways in which the above inferences have been attempted, and evaluate the strength of support that each approach can provide. This methodological assessment sets the stage for 11 accompanying review articles that attempt comprehensive syntheses of what is currently known – and not known – about responses to climate change in a variety of taxa and in theory. Summarizing and relying on the results of these reviews, we arrive at the conclusion that evidence for genetic adaptation to climate change has been found in some systems, but is still relatively scarce. Most importantly, it is clear that more studies are needed – and these must employ better inferential methods – before general conclusions can be drawn. Overall, we hope that the present paper and special issue provide inspiration for future research and guidelines on best practices for its execution.

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          The strength of phenotypic selection in natural populations.

          How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.
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            Climate change and evolution: disentangling environmental and genetic responses.

            Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate-mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often - if not typically - based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long-term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear-cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.
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              A quantitative survey of local adaptation and fitness trade-offs.

              The long history of reciprocal transplant studies testing the hypothesis of local adaptation has shown that populations are often adapted to their local environments. Yet many studies have not demonstrated local adaptation, suggesting that sometimes native populations are no better adapted than are genotypes from foreign environments. Local adaptation may also lead to trade-offs, in which adaptation to one environment comes at a cost of adaptation to another environment. I conducted a survey of published studies of local adaptation to quantify its frequency and magnitude and the costs associated with local adaptation. I also quantified the relationship between local adaptation and environmental differences and the relationship between local adaptation and phenotypic divergence. The overall frequency of local adaptation was 0.71, and the magnitude of the native population advantage in relative fitness was 45%. Divergence between home site environments was positively associated with the magnitude of local adaptation, but phenotypic divergence was not. I found a small negative correlation between a population's relative fitness in its native environment and its fitness in a foreign environment, indicating weak trade-offs associated with local adaptation. These results suggest that populations are often locally adapted but stochastic processes such as genetic drift may limit the efficacy of divergent selection.
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                Author and article information

                Journal
                Evol Appl
                Evol Appl
                eva
                Evolutionary Applications
                Blackwell Publishing Ltd
                1752-4571
                1752-4571
                January 2014
                08 January 2014
                : 7
                : 1
                : 1-14
                Affiliations
                [1 ]Ecological Genetics Research Unit, Department of Biosciences, University of Helsinki Helsinki, Finland
                [2 ]Redpath Museum & Department of Biology, McGill University Montreal, QC, Canada
                Author notes
                Juha Merilä, Ecological Genetics Research Unit, Department of Biosciences, University of Helsinki, PO Box 65, FIN-00014 Helsinki, Finland. Tel.: +358 40 8374165; fax: +358 9 19157694; e-mail: juha.merilä@ 123456helsinki.fi
                [*]

                Authors contributed equally.

                Article
                10.1111/eva.12137
                3894893
                24454544
                1ef4ece5-5688-45dc-8fd9-c3349b558778
                © 2013 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 02 November 2013
                : 08 November 2013
                Categories
                Perspective

                Evolutionary Biology
                genetics,evolution,individual plasticity,environmental change,natural selection,global change

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