Adaptive responses of animals to climate change are most likely insufficient
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, metaanalýza, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S., systematický přehled
PubMed
31337752
PubMed Central
PMC6650445
DOI
10.1038/s41467-019-10924-4
PII: 10.1038/s41467-019-10924-4
Knihovny.cz E-zdroje
- MeSH
- aklimatizace fyziologie MeSH
- časové faktory MeSH
- fenotyp * MeSH
- klimatické změny * MeSH
- ptáci fyziologie MeSH
- selekce (genetika) fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- metaanalýza MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- systematický přehled MeSH
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.
A Skyline Drive Corning NY 14830 USA
Biodiversity research Systematic Botany University of Potsdam Maulbeerallee 1 Berlin 14469 Germany
Centre for Ecology and Hydrology Bush Estate Penicuik EH26 0QB UK
CREAF 08193 Cerdanyola del Vallès Spain
CSIC Global Ecology Unit CREAF CSIC UAB Bellaterra 08193 Spain
Departamento de Zoologia Facultad de Ciencias Universidad de Granada 18071 Granada Spain
Department of Anatomy Cellular Biology and Zoology University of Extremadura 06006 Badajoz Spain
Department of Biological Sciences Auburn University Auburn AL 36849 USA
Department of Biological Sciences University of Texas Rio Grande Valley Brownsville 78520 TX USA
Department of Biology Lund University 22362 Lund Sweden
Department of Biology University of Ottawa Ontario K1N 6N5 Canada
Department of Biology University of Turku Turku FI 20014 Finland
Department of Ecology Evolution and Organismal Biology Iowa State University Ames IA 50011 USA
Department of Ecology Technische Universität Berlin 12165 Berlin Germany
Department of Forest and Conservation Sciences 2424 Main Mall Vancouver V6T 1Z4 BC Canada
Department of Zoology Palacký University tř 17 listopadu 50 771 46 Olomouc Czech Republic
Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK
Edward Grey Institute Department of Zoology University of Oxford Oxford OX1 3PS UK
Estonian University of Life Sciences Kreutzwaldi 5 51014 Tartu Estonia
Evolutionary Ecology Group University of Antwerp Universiteitsplein 1 2610 Wilrijk Belgium
Imperial College London Silwood Park Campus Buckurst Road Ascot SL5 7PY UK
Institute of Zoology Poznan University of Life Sciences Wojska Polskiego 71C 60 625 Poznań Poland
ISEM Université de Montpellier CNRS IRD EPHE Montpellier 34095 France
Lab of Ornithology Cornell University Ithaca NY 14850 USA
Leibniz Institute for Zoo and Wildlife Research Alfred Kowalke Straße 17 10315 Berlin Germany
LPO Mission Rapaces 26 avenue Alain Guigue 13104 Mas Thibert France
Miromiro Drive Kaikoura 7300 New Zealand
Museu de Ciències Naturals de Barcelona P° Picasso s n Parc Ciutadella 08003 Barcelona Spain
Natural History Museum of Granollers Francesc Macià 52 08401 Granollers Spain
Norwegian Institute for Nature Research P O Box 5685 Torgarden 7485 Trondheim Norway
Savannah River Ecology Laboratory University of Georgia Aiken SC 29802 USA
School of Biological Earth and Environmental Sciences University College Cork Cork T23 N73K Ireland
School of Biology Faculty of Biological Sciences University of Leeds Leeds LS2 9JT UK
Swedish Museum of Natural History P O Box 50007 10405 Stockholm Sweden
Zobrazit více v PubMed
Sakschewski B, et al. Resilience of Amazon forests emerges from plant trait diversity. Nat. Clim. Chang. 2016;6:1032–1036. doi: 10.1038/nclimate3109. DOI
Pacifici M, et al. Species’ traits influenced their response to recent climate change. Nat. Clim. Chang. 2017;7:205–208. doi: 10.1038/nclimate3223. DOI
Thomas CD, et al. Extinction risk from climate change. Nature. 2004;427:145–148. doi: 10.1038/nature02121. PubMed DOI
Schindler DE, Hilborn R. Prediction, precaution, and policy under global change. Science. 2015;347:953–954. doi: 10.1126/science.1261824. PubMed DOI
Urban MC, et al. Improving the forecast for biodiversity under climate change. Science. 2016;353:1113–1122. doi: 10.1126/science.aaf4802. PubMed DOI
Hoffmann AA, Sgrò CM. Climate change and evolutionary adaptation. Nature. 2011;470:479–485. doi: 10.1038/nature09670. PubMed DOI
Charmantier A, et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science. 2008;320:800–803. doi: 10.1126/science.1157174. PubMed DOI
van Gils JA, et al. Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range. Science. 2016;352:819–821. doi: 10.1126/science.aad6351. PubMed DOI
Post E, Forchhammer MC. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos. Trans. R. Soc. Ser. B. 2008;363:2367–2373. doi: 10.1098/rstb.2007.2207. PubMed DOI PMC
Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 2008;17:167–178. doi: 10.1111/j.1365-294X.2007.03413.x. PubMed DOI
Merilä J, Hendry AP. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 2014;7:1–14. doi: 10.1111/eva.12137. PubMed DOI PMC
Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37–42. doi: 10.1038/nature01286. PubMed DOI
Thackeray SJ, et al. Phenological sensitivity to climate across taxa and trophic levels. Nature. 2016;535:241–245. doi: 10.1038/nature18608. PubMed DOI
Yom-Tov Y, Yom-Tov S, Wright J, Thorne CJR, Du Feu R. Recent changes in body weight and wing length among some British passerine birds. Oikos. 2006;112:91–101. doi: 10.1111/j.0030-1299.2006.14183.x. DOI
Intergovernmental Panel on Climate Change, editor. Climate Change 2013 - The Physical Science Basis. Cambridge: Cambridge University Press; 2009.
Parmesan C. Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Chang. Biol. 2007;13:1860–1872. doi: 10.1111/j.1365-2486.2007.01404.x. DOI
Cohen Jeremy M., Lajeunesse Marc J., Rohr Jason R. A global synthesis of animal phenological responses to climate change. Nature Climate Change. 2018;8(3):224–228. doi: 10.1038/s41558-018-0067-3. DOI
Poloczanska ES, et al. Global imprint of climate change on marine life. Nat. Clim. Chang. 2013;3:919–925. doi: 10.1038/nclimate1958. DOI
Gotanda KM, Correa C, Turcotte MM, Rolshausen G, Hendry AP. Linking macrotrends and microrates: re-evaluating microevolutionary support for Cope’s rule. Evolution. 2015;69:1345–1354. doi: 10.1111/evo.12653. PubMed DOI
Teplitsky C, Millien V. Climate warming and Bergmann’s rule through time: is there any evidence? Evol. Appl. 2014;7:156–168. doi: 10.1111/eva.12129. PubMed DOI PMC
Kattge J, et al. TRY—a global database of plant traits. Glob. Chang. Biol. 2011;17:2905–2935. doi: 10.1111/j.1365-2486.2011.02451.x. DOI
Salguero-Gómez R, et al. COMADRE: a global data base of animal demography. J. Anim. Ecol. 2016;85:371–384. doi: 10.1111/1365-2656.12482. PubMed DOI PMC
Jones KE, et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology. 2009;90:2648–2648. doi: 10.1890/08-1494.1. DOI
Kingsolver JG, et al. The strength of phenotypic selection in natural populations. Am. Nat. 2001;157:245–261. doi: 10.1086/319193. PubMed DOI
Kingsolver JG, Diamond SE. Phenotypic selection in natural populations: what limits directional selection? Am. Nat. 2011;177:346–357. doi: 10.1086/658341. PubMed DOI
Siepielski AM, DiBattista JD, Carlson SM. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 2009;12:1261–1276. doi: 10.1111/j.1461-0248.2009.01381.x. PubMed DOI
Siepielski AM, et al. Precipitation drives global variation in natural selection. Science. 2017;355:959–962. doi: 10.1126/science.aag2773. PubMed DOI
Caruso CM, et al. What are the environmental determinants of phenotypic selection? A meta-analysis of experimental studies. Am. Nat. 2017;190:363–376. doi: 10.1086/692760. PubMed DOI
Lande R, Arnold SJ. The measurement of selection on correlated characters. Evolution. 1983;37:1210–1226. doi: 10.1111/j.1558-5646.1983.tb00236.x. PubMed DOI
Brown CJ, et al. Ecological and methodological drivers of species’ distribution and phenology responses to climate change. Glob. Chang. Biol. 2016;22:1548–1560. doi: 10.1111/gcb.13184. PubMed DOI
Post, E., Steinman, B. A. & Mann, M. E. Acceleration of phenological advance and warming with latitude over the past century. Sci. Rep. 8, 10.1038/s41598-018-22258-0 (2018). PubMed PMC
Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P. Bird migration times, climate change, and changing population sizes. Glob. Chang. Biol. 2008;14:1959–1972. doi: 10.1111/j.1365-2486.2008.01619.x. DOI
Intergovernmental Panel on Climate Change, editor. Climate Change 2013 - The Physical Science Basis. Cambridge: Cambridge University Press; 2009.
Kharouba Heather M., Ehrlén Johan, Gelman Andrew, Bolmgren Kjell, Allen Jenica M., Travers Steve E., Wolkovich Elizabeth M. Global shifts in the phenological synchrony of species interactions over recent decades. Proceedings of the National Academy of Sciences. 2018;115(20):5211–5216. doi: 10.1073/pnas.1714511115. PubMed DOI PMC
Bϋrger R, Lynch M. Evolution and extinction in a changing environment—a quantitative-genetic analysis. Evolution. 1995;49:151–163. doi: 10.1111/j.1558-5646.1995.tb05967.x. PubMed DOI
Chevin Luis-Miguel, Lande Russell, Mace Georgina M. Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory. PLoS Biology. 2010;8(4):e1000357. doi: 10.1371/journal.pbio.1000357. PubMed DOI PMC
Estes S, Arnold SJ. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 2007;169:227–244. doi: 10.1086/510633. PubMed DOI
VanDerWal J, et al. Focus on poleward shifts in species’ distribution underestimates the fingerprint of climate change. Nat. Clim. Chang. 2012;3:239–243. doi: 10.1038/nclimate1688. DOI
Devictor V, et al. Differences in the climatic debts of birds and butterflies at a continental scale. Nat. Clim. Chang. 2012;2:121–124. doi: 10.1038/nclimate1347. DOI
Parmesan C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 2006;37:637–669. doi: 10.1146/annurev.ecolsys.37.091305.110100. DOI
Pierson JC, et al. Incorporating evolutionary processes into population viability models. Conserv. Biol. 2015;29:755–764. doi: 10.1111/cobi.12431. PubMed DOI
Schiffers KH, Travis JMJ. ALADYN—a spatially explicit, allelic model for simulating adaptive dynamics. Ecography J. 2014;37:1288–1291. doi: 10.1111/ecog.00680. PubMed DOI PMC
Socolar Jacob B., Epanchin Peter N., Beissinger Steven R., Tingley Morgan W. Phenological shifts conserve thermal niches in North American birds and reshape expectations for climate-driven range shifts. Proceedings of the National Academy of Sciences. 2017;114(49):12976–12981. doi: 10.1073/pnas.1705897114. PubMed DOI PMC
Reed TE, Grøtan V, Jenouvrier S, Sæther B-E, Visser ME. Population growth in a wild bird is buffered against phenological mismatch. Science. 2013;340:488–491. doi: 10.1126/science.1232870. PubMed DOI
Rausher MD. The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution (N. Y). 1992;46:616–626. PubMed
Vedder Oscar, Bouwhuis Sandra, Sheldon Ben C. Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations. PLoS Biology. 2013;11(7):e1001605. doi: 10.1371/journal.pbio.1001605. PubMed DOI PMC
Burrows Michael T., Schoeman David S., Richardson Anthony J., Molinos Jorge García, Hoffmann Ary, Buckley Lauren B., Moore Pippa J., Brown Christopher J., Bruno John F., Duarte Carlos M., Halpern Benjamin S., Hoegh-Guldberg Ove, Kappel Carrie V., Kiessling Wolfgang, O’Connor Mary I., Pandolfi John M., Parmesan Camille, Sydeman William J., Ferrier Simon, Williams Kristen J., Poloczanska Elvira S. Geographical limits to species-range shifts are suggested by climate velocity. Nature. 2014;507(7493):492–495. doi: 10.1038/nature12976. PubMed DOI
Torda G, et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Chang. 2017;7:627–636. doi: 10.1038/nclimate3374. DOI
Kruuk LEB. Estimating genetic parameters in natural populations using the ‘animal model’. Philos. Trans. R. Soc. Lond. Ser. B. 2004;359:873–890. doi: 10.1098/rstb.2003.1437. PubMed DOI PMC
Courtiol A, Tropf FC, Mills MC. When genes and environment disagree: Making sense of trends in recent human evolution. Proc. Natl. Acad. Sci. USA. 2016;113:7693–7695. doi: 10.1073/pnas.1608532113. PubMed DOI PMC
Kruuk LEB, Merilä J, Sheldon BC. When environmental variation short-circuits natural selection. Trends Ecol. Evol. 2003;18:207–209. doi: 10.1016/S0169-5347(03)00073-9. DOI
Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37. doi: 10.1038/nature01286. PubMed DOI
Lane JE, Kruuk LEB, Charmantier A, Murie JO, Dobson FS. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature. 2012;489:554–557. doi: 10.1038/nature11335. PubMed DOI
Miles WTS, et al. Quantifying full phenological event distributions reveals simultaneous advances, temporal stability and delays in spring and autumn migration timing in long-distance migratory birds. Glob. Chang. Biol. 2017;23:1400–1414. doi: 10.1111/gcb.13486. PubMed DOI
Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 2011;26:285–291. doi: 10.1016/j.tree.2011.03.005. PubMed DOI
Sheridan JA, Bickford D. Shrinking body size as an ecological response to climate change. Nat. Clim. Chang. 2011;1:401–406. doi: 10.1038/nclimate1259. DOI
Meiri S, Guy D, Dayan T, Simberloff D. Global change and carnivore body size: data are stasis. Glob. Ecol. Biogeogr. 2009;18:240–247. doi: 10.1111/j.1466-8238.2008.00437.x. DOI
Vasseur DA, et al. Increased temperature variation poses a greater risk to species than climate warming. Proc. Biol. Sci. 2014;281:20132612. doi: 10.1098/rspb.2013.2612. PubMed DOI PMC
McLean N, Lawson CR, Leech DI, van de Pol M. Predicting when climate-driven phenotypic change affects population dynamics. Ecol. Lett. 2016;19:595–608. doi: 10.1111/ele.12599. PubMed DOI
Coulson T, et al. Modelling adaptive and nonadaptive responses of populations to environmental change. Am. Nat. 2017;3:313–336. doi: 10.1086/692542. PubMed DOI
Lajeunesse MJ. Facilitating systematic reviews, data extraction and meta-analysis with the metagear package for R. Methods Ecol. Evol. 2016;7:323–330. doi: 10.1111/2041-210X.12472. DOI
Vaida F, Blanchard S. Conditional Akaike information for mixed-effects models. Biometrika. 2005;92:351–370. doi: 10.1093/biomet/92.2.351. DOI
R. Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).
Rousset F, Ferdy J-B. Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography J. 2014;37:781–790. doi: 10.1111/ecog.00566. DOI
Koricheva, J., Gurevitch, J. & Mengersen, K. Handbook of Meta-analysis in Ecology and Evolution (Princeton University Press, Englewood Cliffs, 2013).
Goodenough AE, Hart AG, Elliot SL. What prevents phenological adjustment to climate change in migrant bird species? Evidence against the ‘arrival constraint’ hypothesis. Int. J. Biometeorol. 2011;55:97–102. doi: 10.1007/s00484-010-0312-6. PubMed DOI
Plard Floriane, Gaillard Jean-Michel, Coulson Tim, Hewison A. J. Mark, Delorme Daniel, Warnant Claude, Bonenfant Christophe. Mismatch Between Birth Date and Vegetation Phenology Slows the Demography of Roe Deer. PLoS Biology. 2014;12(4):e1001828. doi: 10.1371/journal.pbio.1001828. PubMed DOI PMC
Gienapp P, et al. Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Philos. Trans. R. Soc. Ser. B. 2012;368:20120289–20120289. doi: 10.1098/rstb.2012.0289. PubMed DOI PMC
Wilson S, Norris DR, Wilson AG, Arcese P. Breeding experience and population density affect the ability of a songbird to respond to future climate variation. Proc. R. Soc. Ser. B. 2007;274:2539–2545. doi: 10.1098/rspb.2007.0643. PubMed DOI PMC
Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub