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      The environmental genomics of metazoan thermal adaptation

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          Abstract

          Continued and accelerating change in the thermal environment places an ever-greater priority on understanding how organisms are going to respond. The paradigm of ‘move, adapt or die', regarding ways in which organisms can respond to environmental stressors, stimulates intense efforts to predict the future of biodiversity. Assuming that extinction is an unpalatable outcome, researchers have focussed attention on how organisms can shift in their distribution to stay in the same thermal conditions or can stay in the same place by adapting to a changing thermal environment. How likely these respective outcomes might be depends on the answer to a fundamental evolutionary question, namely what genetic changes underpin adaptation to the thermal environment. The increasing access to and decreasing costs of next-generation sequencing (NGS) technologies, which can be applied to both model and non-model systems, provide a much-needed tool for understanding thermal adaptation. Here we consider broadly what is already known from non-NGS studies about thermal adaptation, then discuss the benefits and challenges of different NGS methodologies to add to this knowledge base. We then review published NGS genomics and transcriptomics studies of thermal adaptation to heat stress in metazoans and compare these results with previous non-NGS patterns. We conclude by summarising emerging patterns of genetic response and discussing future directions using these increasingly common techniques.

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          The genomic basis of adaptive evolution in threespine sticklebacks

          Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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            Climate change, adaptation, and phenotypic plasticity: the problem and the evidence

            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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              Chromosome inversions, local adaptation and speciation.

              We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.
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                Author and article information

                Journal
                Heredity (Edinb)
                Heredity (Edinb)
                Heredity
                Nature Publishing Group
                0018-067X
                1365-2540
                May 2015
                04 March 2015
                1 May 2015
                : 114
                : 5
                : 502-514
                Affiliations
                [1 ]Department of Animal and Plant Sciences, University of Sheffield , Sheffield, UK
                [2 ]Sven Lovén Centre—Tjärnö, University of Gothenburg , Strömstad, Sweden
                [3 ]Environment and Sustainability Institute, University of Exeter , Penryn, UK
                [4 ]Laboratoire Evolution, Génomes et Spéciation, CNRS—UPR 9034 , Gif sur Yvette, France
                [5 ]Université Paris-Sud , Orsay, France
                Author notes
                [* ]Department of Animal and Plant Sciences, University of Sheffield , Western Bank, Sheffield S10 2TN, UK. E-mail: d.porcelli@ 123456sheffield.ac.uk
                Article
                hdy2014119
                10.1038/hdy.2014.119
                4815515
                25735594
                8f7c1596-1605-45f6-b0d6-ad771cb95e70
                Copyright © 2015 The Genetics Society

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 22 May 2014
                : 06 November 2014
                : 11 November 2014
                Categories
                Review

                Human biology
                Human biology

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