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      Adaptation of plasticity to projected maximum temperatures and across climatically defined bioregions

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          Significance

          Adaptation to climate change is expected to be influenced by thermal conditions experienced by species during their evolutionary history. We studied plastic capacity as a target of climatic selection, hypothesizing that populations that evolved under warmer climates have greater plastic adaptive resilience to climate change. This was tested experimentally by comparing upper thermal tolerance and gene expression in fish populations from desert, temperate, and subtropical regions of Australia. Divergent adaptive plastic responses to future climates were found across different bioregions, including in key heat stress genes. The greatest adaptive resilience was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. These results have implications for large-scale assessments of climate impacts and for predictions of species distribution changes.

          Abstract

          Resilience to environmental stressors due to climate warming is influenced by local adaptations, including plastic responses. The recent literature has focused on genomic signatures of climatic adaptation, but little is known about how plastic capacity may be influenced by biogeographic and evolutionary processes. We investigate phenotypic plasticity as a target of climatic selection, hypothesizing that lineages that evolved in warmer climates will exhibit greater plastic adaptive resilience to upper thermal stress. This was experimentally tested by comparing transcriptomic responses within and among temperate, subtropical, and desert ecotypes of Australian rainbowfish subjected to contemporary and projected summer temperatures. Critical thermal maxima were estimated, and ecological niches delineated using bioclimatic modeling. A comparative phylogenetic expression variance and evolution model was used to assess plastic and evolved changes in gene expression. Although 82% of all expressed genes were found in the three ecotypes, they shared expression patterns in only 5 out of 236 genes that responded to the climate change experiment. A total of 532 genes showed signals of adaptive (i.e., genetic-based) plasticity due to ecotype-specific directional selection, and 23 of those responded to projected summer temperatures. Network analyses demonstrated centrality of these genes in thermal response pathways. The greatest adaptive resilience to upper thermal stress was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. Our findings indicate that vulnerability to climate change will be highly influenced by biogeographic factors, emphasizing the value of integrative assessments of climatic adaptive traits for accurate estimation of population and ecosystem responses.

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          Most cited references 71

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          Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology.

          Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
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            Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments

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              Poleward shifts in geographical ranges of butterfly species associated with regional warming

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                21 July 2020
                9 July 2020
                9 July 2020
                : 117
                : 29
                : 17112-17121
                Affiliations
                aMolecular Ecology Lab, Flinders University , Bedford Park, SA 5042, Australia;
                bKonrad Lorenz Institute of Ethology, University of Veterinary Medicine , 1160 Vienna, Austria;
                cInstitut de Biologie Intégrative et des Systèmes, Université Laval, Québec , QC G1V 0A6, Canada
                Author notes
                1To whom correspondence may be addressed. Email: luciano.beheregaray@ 123456flinders.edu.au .

                Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved June 2, 2020 (received for review December 2, 2019)

                Author contributions: L.B. and L.B.B. designed research; J.S.-C., K.G., C.J.B., S.S., L.B., and L.B.B. performed research; L.B.B. contributed new reagents/analytic tools; J.S.-C., C.J.B., and S.S. analyzed data; and J.S.-C., K.G., and L.B.B. wrote the paper.

                Article
                201921124
                10.1073/pnas.1921124117
                7382230
                32647058
                Copyright © 2020 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                Page count
                Pages: 10
                Product
                Funding
                Funded by: Australian Research Council (ARC) 501100000923
                Award ID: DP110101207
                Award Recipient : Louis Bernatchez Award Recipient : Luciano B Beheregaray
                Funded by: Australian Research Council (ARC) 501100000923
                Award ID: DP150102903
                Award Recipient : Louis Bernatchez Award Recipient : Luciano B Beheregaray
                Funded by: Australian Research Council (ARC) 501100000923
                Award ID: FT130101068
                Award Recipient : Louis Bernatchez Award Recipient : Luciano B Beheregaray
                Categories
                Biological Sciences
                Evolution

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