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Title: Adaptive responses of animals to climate change are most likely insufficient

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.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [3]; ORCiD logo [5]; ORCiD logo [6];  [7];  [8];  [9];  [10];  [11]; ORCiD logo [12];  [13];  [14];  [15];  [7];  [16];  [17]; ORCiD logo [18] more »; ORCiD logo [19];  [20]; ORCiD logo [21];  [22]; ORCiD logo [23];  [24]; ORCiD logo [25]; ORCiD logo [26];  [14];  [26];  [27]; ORCiD logo [28];  [29];  [30];  [31]; ;  [16];  [32];  [33];  [16];  [34];  [7]; ORCiD logo [3];  [35]; ORCiD logo [36];  [13];  [37];  [38];  [39];  [26];  [40]; ORCiD logo [41]; ORCiD logo [42]; ORCiD logo [1];  [43]; ORCiD logo [44];  [45]; ORCiD logo [46];  [7]; ORCiD logo [47];  [48]; ORCiD logo [4];  [49]; ORCiD logo [1]; ORCiD logo [50] « less
+ Show Author Affiliations
  1. Leibniz Inst. for Zoo and Wildlife Research, Berlin (Germany)
  2. Univ. College Cork (Ireland)
  3. Univ. de Montpellier (France)
  4. Netherlands Inst. of Ecology, Wageningen (Netherlands)
  5. Univ. of Leeds, Leeds (United Kingdom)
  6. Palacký Univ., Olomouc (Czech Republic)
  7. Univ. of Antwerp (Belgium)
  8. Swedish Museum of Natural History, Stockholm (Sweden)
  9. Department of Forest and Conservation Sciences, Vancouver, BC (Canada)
  10. Experimental Station of Arid Zones, Almeria (Spain)
  11. Univ. of Seville (Spain)
  12. Univ. of Texas Rio Grande Valley, Brownsville, TX (United States)
  13. Museu de Ciències Naturals de Barcelona (Spain)
  14. Bush Estate, Penicuik (United Kingdom)
  15. Univ. Paul Sabatier, Moulis (France)
  16. Univ. of Extremadura, Badajoz (Spain)
  17. Cornell Univ., Ithaca, NY (United States)
  18. Ludwig Maximilian Univ., Munich (Germany)
  19. Univ. of Hyogo, Kobe (Japan)
  20. Univ. of Turku (Finland)
  21. Leibniz Inst. for Zoo and Wildlife Research, Berlin (Germany); Potsdam Univ. (Germany)
  22. CREAF, Cerdanyola del Vallès (Spain); Consejo Superior de Investigaciones Cientificas (CSIC), Bellaterra (Spain)
  23. Norwegian Inst. for Nature Research (NINA), Trondheim (Norway); Norwegian Univ. of Science and Technology, Trondheim (Norway)
  24. Univ. of Gloucestershire (United Kingdom)
  25. Estonian Univ. of Life Sciences, Tartu (Estonia)
  26. Lund Univ. (Sweden)
  27. Senckenberg Biodiversity and Climate Research Center (BiK-F). Frankfurt (Germany)
  28. Univ. of Potsdam (Germany); HSR Hochschule für Technik, Rapperswil (Switzerland)
  29. Univ. of Ottawa, ON (Canada)
  30. Univ. of Granada (Spain)
  31. Sorbonne Univ., Paris (France)
  32. Consejo Superior de Investigaciones Cientificas (CSIC), Bellaterra (Spain)
  33. Univ. of Zurich (Switzerland)
  34. LPO Mission Rapaces, Mas-Thibert (France)
  35. Museum für Naturkunde, Berlin (Germany)
  36. Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)
  37. CREAF, Cerdanyola del Vallès (Spain); Natural History Museum of Granollers (Spain)
  38. Consejo Superior de Investigaciones Cientificas (CSIC), Bellaterra (Spain); Norwegian Inst. for Nature Research (NINA), Trondheim (Norway)
  39. Tokyo Metropolitan Univ. (Japan)
  40. Univ. of Wyoming, Laramie, WY (United States)
  41. Potsdam Inst. for Climate Impact Research (PIK) (Germany)
  42. Imperial College, London (United Kingdom); Univ. of Cambridge (United Kingdom)
  43. Poznan Univ. of Life Sciences (Poland)
  44. Univ. of Helsinki (Finland)
  45. Univ. of Oxford (United Kingdom)
  46. Universite Paris-Saclay, Orsay (France)
  47. Iowa State Univ., Ames, IA (United States)
  48. Auburn Univ., AL (United States)
  49. Univ. of California, Berkeley, CA (United States)
  50. Leibniz Inst. for Zoo and Wildlife Research, Berlin (Germany); Technical Univ. of Berlin (Germany)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Environmental Management (EM)
OSTI Identifier:
1614670
Grant/Contract Number:  
FC09-07SR22506
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Radchuk, Viktoriia, Reed, Thomas, Teplitsky, Céline, van de Pol, Martijn, Charmantier, Anne, Hassall, Christopher, Adamík, Peter, Adriaensen, Frank, Ahola, Markus P., Arcese, Peter, Miguel Avilés, Jesús, Balbontin, Javier, Berg, Karl S., Borras, Antoni, Burthe, Sarah, Clobert, Jean, Dehnhard, Nina, de Lope, Florentino, Dhondt, André A., Dingemanse, Niels J., Doi, Hideyuki, Eeva, Tapio, Fickel, Joerns, Filella, Iolanda, Fossøy, Frode, Goodenough, Anne E., Hall, Stephen J. G., Hansson, Bengt, Harris, Michael, Hasselquist, Dennis, Hickler, Thomas, Joshi, Jasmin, Kharouba, Heather, Martínez, Juan Gabriel, Mihoub, Jean-Baptiste, Mills, James A., Molina-Morales, Mercedes, Moksnes, Arne, Ozgul, Arpat, Parejo, Deseada, Pilard, Philippe, Poisbleau, Maud, Rousset, Francois, Rödel, Mark-Oliver, Scott, David, Senar, Juan Carlos, Stefanescu, Constanti, Stokke, Bård G., Kusano, Tamotsu, Tarka, Maja, Tarwater, Corey E., Thonicke, Kirsten, Thorley, Jack, Wilting, Andreas, Tryjanowski, Piotr, Merilä, Juha, Sheldon, Ben C., Pape Møller, Anders, Matthysen, Erik, Janzen, Fredric, Dobson, F. Stephen, Visser, Marcel E., Beissinger, Steven R., Courtiol, Alexandre, and Kramer-Schadt, Stephanie. Adaptive responses of animals to climate change are most likely insufficient. United States: N. p., 2019. Web. doi:10.1038/s41467-019-10924-4.
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Radchuk, Viktoriia, Reed, Thomas, Teplitsky, Céline, van de Pol, Martijn, Charmantier, Anne, Hassall, Christopher, Adamík, Peter, Adriaensen, Frank, Ahola, Markus P., Arcese, Peter, Miguel Avilés, Jesús, Balbontin, Javier, Berg, Karl S., Borras, Antoni, Burthe, Sarah, Clobert, Jean, Dehnhard, Nina, de Lope, Florentino, Dhondt, André A., Dingemanse, Niels J., Doi, Hideyuki, Eeva, Tapio, Fickel, Joerns, Filella, Iolanda, Fossøy, Frode, Goodenough, Anne E., Hall, Stephen J. G., Hansson, Bengt, Harris, Michael, Hasselquist, Dennis, Hickler, Thomas, Joshi, Jasmin, Kharouba, Heather, Martínez, Juan Gabriel, Mihoub, Jean-Baptiste, Mills, James A., Molina-Morales, Mercedes, Moksnes, Arne, Ozgul, Arpat, Parejo, Deseada, Pilard, Philippe, Poisbleau, Maud, Rousset, Francois, Rödel, Mark-Oliver, Scott, David, Senar, Juan Carlos, Stefanescu, Constanti, Stokke, Bård G., Kusano, Tamotsu, Tarka, Maja, Tarwater, Corey E., Thonicke, Kirsten, Thorley, Jack, Wilting, Andreas, Tryjanowski, Piotr, Merilä, Juha, Sheldon, Ben C., Pape Møller, Anders, Matthysen, Erik, Janzen, Fredric, Dobson, F. Stephen, Visser, Marcel E., Beissinger, Steven R., Courtiol, Alexandre, & Kramer-Schadt, Stephanie. Adaptive responses of animals to climate change are most likely insufficient. United States. https://doi.org/10.1038/s41467-019-10924-4
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Radchuk, Viktoriia, Reed, Thomas, Teplitsky, Céline, van de Pol, Martijn, Charmantier, Anne, Hassall, Christopher, Adamík, Peter, Adriaensen, Frank, Ahola, Markus P., Arcese, Peter, Miguel Avilés, Jesús, Balbontin, Javier, Berg, Karl S., Borras, Antoni, Burthe, Sarah, Clobert, Jean, Dehnhard, Nina, de Lope, Florentino, Dhondt, André A., Dingemanse, Niels J., Doi, Hideyuki, Eeva, Tapio, Fickel, Joerns, Filella, Iolanda, Fossøy, Frode, Goodenough, Anne E., Hall, Stephen J. G., Hansson, Bengt, Harris, Michael, Hasselquist, Dennis, Hickler, Thomas, Joshi, Jasmin, Kharouba, Heather, Martínez, Juan Gabriel, Mihoub, Jean-Baptiste, Mills, James A., Molina-Morales, Mercedes, Moksnes, Arne, Ozgul, Arpat, Parejo, Deseada, Pilard, Philippe, Poisbleau, Maud, Rousset, Francois, Rödel, Mark-Oliver, Scott, David, Senar, Juan Carlos, Stefanescu, Constanti, Stokke, Bård G., Kusano, Tamotsu, Tarka, Maja, Tarwater, Corey E., Thonicke, Kirsten, Thorley, Jack, Wilting, Andreas, Tryjanowski, Piotr, Merilä, Juha, Sheldon, Ben C., Pape Møller, Anders, Matthysen, Erik, Janzen, Fredric, Dobson, F. Stephen, Visser, Marcel E., Beissinger, Steven R., Courtiol, Alexandre, and Kramer-Schadt, Stephanie. Tue . "Adaptive responses of animals to climate change are most likely insufficient". United States. https://doi.org/10.1038/s41467-019-10924-4. https://www.osti.gov/servlets/purl/1614670.
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@article{osti_1614670,
title = {Adaptive responses of animals to climate change are most likely insufficient},
author = {Radchuk, Viktoriia and Reed, Thomas and Teplitsky, Céline and van de Pol, Martijn and Charmantier, Anne and Hassall, Christopher and Adamík, Peter and Adriaensen, Frank and Ahola, Markus P. and Arcese, Peter and Miguel Avilés, Jesús and Balbontin, Javier and Berg, Karl S. and Borras, Antoni and Burthe, Sarah and Clobert, Jean and Dehnhard, Nina and de Lope, Florentino and Dhondt, André A. and Dingemanse, Niels J. and Doi, Hideyuki and Eeva, Tapio and Fickel, Joerns and Filella, Iolanda and Fossøy, Frode and Goodenough, Anne E. and Hall, Stephen J. G. and Hansson, Bengt and Harris, Michael and Hasselquist, Dennis and Hickler, Thomas and Joshi, Jasmin and Kharouba, Heather and Martínez, Juan Gabriel and Mihoub, Jean-Baptiste and Mills, James A. and Molina-Morales, Mercedes and Moksnes, Arne and Ozgul, Arpat and Parejo, Deseada and Pilard, Philippe and Poisbleau, Maud and Rousset, Francois and Rödel, Mark-Oliver and Scott, David and Senar, Juan Carlos and Stefanescu, Constanti and Stokke, Bård G. and Kusano, Tamotsu and Tarka, Maja and Tarwater, Corey E. and Thonicke, Kirsten and Thorley, Jack and Wilting, Andreas and Tryjanowski, Piotr and Merilä, Juha and Sheldon, Ben C. and Pape Møller, Anders and Matthysen, Erik and Janzen, Fredric and Dobson, F. Stephen and Visser, Marcel E. and Beissinger, Steven R. and Courtiol, Alexandre and Kramer-Schadt, Stephanie},
abstractNote = {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.},
doi = {10.1038/s41467-019-10924-4},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {7}
}
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  • Lande, Russell; Arnold, Stevan J.
  • Evolution, Vol. 37, Issue 6
  • DOI: 10.2307/2408842
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    Works referencing / citing this record:

    Long-term phenology of two North American secondary cavity-nesters in response to changing climate conditions
    journal, October 2019

    • Wysner, Tyler E.; Bartlow, Andrew W.; Hathcock, Charles D.
    • The Science of Nature, Vol. 106, Issue 9-10
    • DOI: 10.1007/s00114-019-1650-9

    Shifts in migration phenology under climate change: temperature vs. abundance effects in birds
    journal, February 2020

    Can Arctic seabirds adapt to climate change?
    journal, August 2019

    Hybridization increases population variation during adaptive radiation
    journal, October 2019

    • Grant, Peter R.; Grant, B. Rosemary
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 46
    • DOI: 10.1073/pnas.1913534116

    Extreme temperature drop alters hatching delay, reproductive success, and physiological condition in great tits
    journal, January 2020

    • Glądalski, Michał; Bańbura, Mirosława; Kaliński, Adam
    • International Journal of Biometeorology, Vol. 64, Issue 4
    • DOI: 10.1007/s00484-019-01851-6

    The ‘algebra of evolution’: the Robertson–Price identity and viability selection for body mass in a wild bird population
    journal, March 2020

    • Hajduk, G. K.; Walling, C. A.; Cockburn, A.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1797
    • DOI: 10.1098/rstb.2019.0359

    The role of selection and evolution in changing parturition date in a red deer population.
    text, January 2019

    • Bonnet, Timothée; Morrissey, Michael B.; Morris, Alison
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.69339

    The role of selection and evolution in changing parturition date in a red deer population.
    text, January 2019

    • Bonnet, Timothée; Morrissey, Michael B.; Morris, Alison
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.46692

    Foraging niche shift maintains breeding parameters of a colonial waterbird during range expansion
    journal, February 2020

    • Francesiaz, Charlotte; Yohannes, Elizabeth; Besnard, Aurélien
    • Ecology and Evolution, Vol. 10, Issue 4
    • DOI: 10.1002/ece3.6030

    The role of selection and evolution in changing parturition date in a red deer population
    journal, November 2019

    Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world
    journal, February 2020

    • González‐Tokman, Daniel; Córdoba‐Aguilar, Alex; Dáttilo, Wesley
    • Biological Reviews, Vol. 95, Issue 3
    • DOI: 10.1111/brv.12588
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