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      Adaptive responses of animals to climate change are most likely insufficient

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      Nature Communications

      Nature Publishing Group UK

      Evolutionary ecology, Climate-change ecology, Conservation biology

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          Abstract

          Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

          Abstract

          It is unclear whether species’ responses to climate change tend to be adaptive or sufficient to keep up with climate change. Here, Radchuk et al. perform a meta-analysis showing that in birds phenology has advanced adaptively in some species, though not all the way to the new optima.

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          Most cited references 43

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          PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals

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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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                Author and article information

                Contributors
                radchuk@izw-berlin.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                23 July 2019
                23 July 2019
                2019
                : 10
                Affiliations
                [1 ]ISNI 0000 0001 0708 0355, GRID grid.418779.4, Leibniz Institute for Zoo and Wildlife Research (IZW), ; Alfred-Kowalke-Straße 17, 10315 Berlin, Germany
                [2 ]ISNI 0000000123318773, GRID grid.7872.a, School of Biological, Earth and Environmental Sciences, , University College Cork, ; Cork, T23 N73K Ireland
                [3 ]CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE, 1919 route de Mende, 34293 Montpellier Cedex 5, France
                [4 ]ISNI 0000 0001 1013 0288, GRID grid.418375.c, Department of Animal Ecology, , Netherlands Institute of Ecology (NIOO-KNAW), ; P.O. Box 50, 6700 AB Wageningen, The Netherlands
                [5 ]ISNI 0000 0004 1936 8403, GRID grid.9909.9, School of Biology, Faculty of Biological Sciences, , University of Leeds, ; Leeds, LS2 9JT UK
                [6 ]ISNI 0000 0001 1245 3953, GRID grid.10979.36, Department of Zoology, , Palacký University, ; tř. 17. listopadu 50, 771 46 Olomouc, Czech Republic
                [7 ]ISNI 0000 0001 0790 3681, GRID grid.5284.b, Evolutionary Ecology Group, , University of Antwerp, ; Universiteitsplein 1, 2610 Wilrijk, Belgium
                [8 ]ISNI 0000 0004 0605 2864, GRID grid.425591.e, Swedish Museum of Natural History, ; P.O. Box 50007, 10405 Stockholm, Sweden
                [9 ]Department of Forest and Conservation Sciences, 2424 Main Mall, Vancouver, V6T 1Z4 BC Canada
                [10 ]ISNI 0000 0004 0547 1725, GRID grid.466639.8, Department of Functional and Evolutionary Ecology, , Experimental Station of Arid Zones (EEZA-CSIC), ; Ctra de Sacramento s/n, 04120 Almería, Spain
                [11 ]ISNI 0000 0001 2168 1229, GRID grid.9224.d, Department of Zoology, Faculty of Biology, , University of Seville, ; Avenue Reina Mercedes, 41012 Seville, Spain
                [12 ]ISNI 0000 0004 5374 269X, GRID grid.449717.8, Department of Biological Sciences, , University of Texas Rio Grande Valley, ; Brownsville, 78520 TX USA
                [13 ]Museu de Ciències Naturals de Barcelona, P° Picasso s/n, Parc Ciutadella, 08003 Barcelona, Spain
                [14 ]Centre for Ecology and Hydrology, Bush Estate, Penicuik, EH26 0QB UK
                [15 ]Station of Experimental and Theoretical Ecology (SETE), UMR 5321, CNRS and University Paul Sabatier, 2 route du CNRS, 09200 Moulis, France
                [16 ]ISNI 0000 0001 0790 3681, GRID grid.5284.b, Behavioural Ecology and Ecophysiology Group, , University of Antwerp, ; Universiteitsplein 1, 2610 Wilrijk (Antwerp), Belgium
                [17 ]ISNI 0000000119412521, GRID grid.8393.1, Department of Anatomy, Cellular Biology and Zoology, , University of Extremadura, ; 06006 Badajoz, Spain
                [18 ]ISNI 000000041936877X, GRID grid.5386.8, Lab of Ornithology, , Cornell University, ; Ithaca, NY 14850 USA
                [19 ]ISNI 0000 0004 1936 973X, GRID grid.5252.0, Behavioural Ecology, Department of Biology, , Ludwig-Maximilians University of Munich, ; Großhaderner Str. 2, Planegg-Martinsried, 82152 Germany
                [20 ]ISNI 0000 0001 0724 9317, GRID grid.266453.0, Graduate School of Simulation Studies, , University of Hyogo, ; 7-1-28 Minatojima-minamimachi, Kobe, 650-0047 Japan
                [21 ]ISNI 0000 0001 2097 1371, GRID grid.1374.1, Department of Biology, , University of Turku, ; Turku, FI-20014 Finland
                [22 ]ISNI 0000 0001 0942 1117, GRID grid.11348.3f, Institute for Biochemistry and Biology, , Potsdam University, ; Karl-Liebknecht-Strasse 24-25, 14476 Potsdam, Germany
                [23 ]ISNI 0000 0001 0722 403X, GRID grid.452388.0, CREAF, ; 08193 Cerdanyola del Vallès, Spain
                [24 ]CSIC, Global Ecology Unit CREAF-CSIC-UAB, Bellaterra, 08193 Spain
                [25 ]ISNI 0000 0001 2107 519X, GRID grid.420127.2, Norwegian Institute for Nature Research (NINA), ; P.O. Box 5685 Torgarden, 7485 Trondheim, Norway
                [26 ]ISNI 0000 0001 1516 2393, GRID grid.5947.f, Department of Biology, , Norwegian University of Science and Technology (NTNU), ; Høgskoleringen 5, 7491 Trondheim, Norway
                [27 ]ISNI 0000000121919137, GRID grid.21027.36, School of Natural and Social Sciences, , University of Gloucestershire, ; Swindon Road, Cheltenham, GL50 4AZ UK
                [28 ]ISNI 0000 0001 0671 1127, GRID grid.16697.3f, Estonian University of Life Sciences, ; Kreutzwaldi 5, 51014 Tartu, Estonia
                [29 ]ISNI 0000 0001 0930 2361, GRID grid.4514.4, Department of Biology, , Lund University, ; 22362 Lund, Sweden
                [30 ]Senckenberg Biodiversity and Climate Research Center (BiK-F), Senckenberganlage 25, 60325 Frankfurt/Main, Germany
                [31 ]ISNI 0000 0001 0942 1117, GRID grid.11348.3f, Biodiversity research/Systematic Botany, , University of Potsdam, ; Maulbeerallee 1, Berlin, 14469 Germany
                [32 ]ISNI 0000 0004 0400 7429, GRID grid.424741.0, Institute for Landscape and Open Space, , HSR Hochschule für Technik, ; Oberseestrasse 10, Rapperswil, 8640 Switzerland
                [33 ]ISNI 0000 0001 2182 2255, GRID grid.28046.38, Department of Biology, , University of Ottawa, ; Ontario, K1N 6N5 Canada
                [34 ]ISNI 0000000121678994, GRID grid.4489.1, Departamento de Zoologia, Facultad de Ciencias, , Universidad de Granada, ; 18071 Granada, Spain
                [35 ]ISNI 0000 0001 2174 9334, GRID grid.410350.3, Sorbonne Université, , Muséum National d’Histoire Naturelle, ; CNRS, CESCO, UMR 7204, 61 rue Buffon, 75005 Paris, France
                [36 ]10527A Skyline Drive, Corning, NY 14830 USA
                [37 ]3 Miromiro Drive, Kaikoura, 7300 New Zealand
                [38 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Department of Evolutionary Biology and Environmental Studies, , University of Zurich, ; Zurich, 8057 Switzerland
                [39 ]LPO Mission Rapaces, 26 avenue Alain Guigue, 13104 Mas-Thibert, France
                [40 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, ISEM, , Université de Montpellier, ; CNRS, IRD, EPHE, Montpellier, 34095 France
                [41 ]ISNI 0000 0001 2293 9957, GRID grid.422371.1, Leibniz Institute for Evolution and Biodiversity Science, , Museum für Naturkunde, ; Invalidenstrasse 43, 10115 Berlin, Germany
                [42 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Savannah River Ecology Laboratory, , University of Georgia, ; Aiken, SC 29802 USA
                [43 ]Natural History Museum of Granollers, Francesc Macià, 52, 08401 Granollers, Spain
                [44 ]ISNI 0000 0001 1090 2030, GRID grid.265074.2, Department of Biological Sciences, , Tokyo Metropolitan University, ; 1-1 Minami-Osawa, Hachioji-shi, Tokyo, 192-0397 Japan
                [45 ]ISNI 0000 0001 2109 0381, GRID grid.135963.b, Department of Zoology and Physiology, , University of Wyoming, ; 1000 E University Avenue, Laramie, WY 82071 USA
                [46 ]ISNI 0000 0004 0493 9031, GRID grid.4556.2, Research Domain 1 ‘Earth System Analysis’, , Potsdam Institute for Climate Impact Research (PIK), ; P.O. Box 60 12 03, Telegrafenberg A31, Potsdam, D-14412 Germany
                [47 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Imperial College London, ; Silwood Park Campus, Buckurst Road, Ascot, SL5 7PY UK
                [48 ]ISNI 0000000121885934, GRID grid.5335.0, Department of Zoology, , University of Cambridge, ; Downing Street, Cambridge, CB2 3EJ UK
                [49 ]ISNI 0000 0001 2157 4669, GRID grid.410688.3, Institute of Zoology, , Poznan University of Life Sciences, ; Wojska Polskiego 71C, 60-625 Poznań, Poland
                [50 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, Organismal and Evolutionary Biology Research Programme, Ecological Genetics Research Unit, Faculty Biological and Environmental Sciences, , University of Helsinki, ; 00014 Helsinki, Finland
                [51 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Edward Grey Institute, Department of Zoology, , University of Oxford, ; Oxford, OX1 3PS UK
                [52 ]ISNI 0000 0004 4910 6535, GRID grid.460789.4, Ecologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech, , Université Paris-Saclay, ; 91405 Orsay Cedex, France
                [53 ]ISNI 0000 0004 1936 7312, GRID grid.34421.30, Department of Ecology, Evolution, and Organismal Biology, , Iowa State University, ; Ames, IA 50011 USA
                [54 ]ISNI 0000 0001 2297 8753, GRID grid.252546.2, Department of Biological Sciences, , Auburn University, ; Auburn, AL 36849 USA
                [55 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Department of Environmental Science, Policy and Management and Museum of Vertebrate Zoology, , University of California, ; Berkeley, 94720 CA USA
                [56 ]ISNI 0000 0001 2292 8254, GRID grid.6734.6, Department of Ecology, , Technische Universität Berlin, ; 12165 Berlin, Germany
                Article
                10924
                10.1038/s41467-019-10924-4
                6650445
                31337752
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef https://doi.org/10.13039/501100000781, EC | European Research Council (ERC);
                Award ID: ERC-2014-StG-639192-ALH
                Award ID: ERC-2013-StG-337365-SHE
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100005876, Suomen Akatemia | Biotieteiden ja Ympäristön Tutkimuksen Toimikunta (Research Council for Biosciences and Environment);
                Award ID: 265859
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001862, Svenska Forskningsrådet Formas (Swedish Research Council Formas);
                Award ID: 621-2014-5222
                Award Recipient :
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                © The Author(s) 2019

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                evolutionary ecology, climate-change ecology, conservation biology

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