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Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change

L. Scott Mills https://orcid.org/0000-0001-8771-509X [email protected], Eugenia V. Bragina https://orcid.org/0000-0001-8791-3619, Alexander V. Kumar https://orcid.org/0000-0003-3831-5924, Marketa Zimova https://orcid.org/0000-0002-8264-9879, Diana J. R. Lafferty https://orcid.org/0000-0001-8938-7130, Jennifer Feltner, Brandon M. Davis https://orcid.org/0000-0003-2013-7875, Klaus Hackländer https://orcid.org/0000-0002-6774-435X, Paulo C. Alves https://orcid.org/0000-0003-4797-0939, Jeffrey M. Good https://orcid.org/0000-0003-0707-5374, José Melo-Ferreira https://orcid.org/0000-0003-4473-1908, Andreas Dietz, Alexei V. Abramov https://orcid.org/0000-0001-9709-4469, Natalia Lopatina https://orcid.org/0000-0003-4660-0936, and Kairsten Fay
Science • 15 Feb 2018 • Vol 359, Issue 6379 • pp. 1033-1036 • DOI: 10.1126/science.aan8097
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Changing coats with the season

Many species of mammals and birds molt from summer brown to winter white coats to facilitate camouflage. Mills et al. mapped global patterns of seasonal coat color change across eight species including hares, weasels, and foxes. They found regions where individuals molt to white, brown, and both white and brown winter coats. Greater proportions of the populations molted to white in higher latitudes. Regions where seasonal coat changes are the most variable (molting to both brown and white) may provide resilience against the warming climate.
Science, this issue p. 1033

Abstract

Maintenance of biodiversity in a rapidly changing climate will depend on the efficacy of evolutionary rescue, whereby population declines due to abrupt environmental change are reversed by shifts in genetically driven adaptive traits. However, a lack of traits known to be under direct selection by anthropogenic climate change has limited the incorporation of evolutionary processes into global conservation efforts. In 21 vertebrate species, some individuals undergo a seasonal color molt from summer brown to winter white as camouflage against snow, whereas other individuals remain brown. Seasonal snow duration is decreasing globally, and fitness is lower for winter white animals on snowless backgrounds. Based on 2713 georeferenced samples of known winter coat color—from eight species across trophic levels—we identify environmentally driven clinal gradients in winter coat color, including polymorphic zones where winter brown and white morphs co-occur. These polymorphic zones, underrepresented by existing global protected area networks, indicate hot spots for evolutionary rescue in a changing climate.
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Supplementary Material

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Figs. S1 to S8
Tables S1 to S6
References (35–46)

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References and Notes

1
J. Huxley, Morphism and evolution. Heredity 9, 1–51 (1955).
2
E. Vander Wal, D. Garant, M. Festa-Bianchet, F. Pelletier, Evolutionary rescue in vertebrates: Evidence, applications and uncertainty. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120090 (2013).
3
M. E. Soulé, O. H. Frankel, Conservation and Evolution (Cambridge Univ. Press, Cambridge, 1981).
4
IUCN, Standard for the identification of key biodiversity areas, Version 1 (IUCN, Gland, Switzerland, 2015).
5
C. R. Margules, R. L. Pressey, Systematic conservation planning. Nature 405, 243–253 (2000).
6
S. Lavergne, M. E. K. Evans, I. J. Burfield, F. Jiguet, W. Thuiller, Are species’ responses to global change predicted by past niche evolution? Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120091 (2013).
7
T. P. Dawson, S. T. Jackson, J. I. House, I. C. Prentice, G. M. Mace, Beyond predictions: Biodiversity conservation in a changing climate. Science 332, 53–58 (2011).
8
A. Gonzalez, O. Ronce, R. Ferriere, M. E. Hochberg, Evolutionary rescue: An emerging focus at the intersection between ecology and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120404 (2013).
9
S. M. Carlson, C. J. Cunningham, P. A. H. Westley, Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530 (2014).
10
N. S. Diffenbaugh, C. B. Field, Changes in ecologically critical terrestrial climate conditions. Science 341, 486–492 (2013).
11
K. E. Kunkel, D. A. Robinson, S. Champion, X. Yin, T. Estilow, R. M. Frankson, Trends and extremes in Northern Hemisphere snow characteristics. Curr. Clim. Change Rep. 2, 65–73 (2016).
12
M. Zimova, L. S. Mills, J. J. Nowak, High fitness costs of climate change-induced camouflage mismatch. Ecol. Lett. 19, 299–307 (2016).
13
S. M. Sultaire, J. N. Pauli, K. J. Martin, M. W. Meyer, M. Notaro, B. Zuckerberg, Climate change surpasses land-use change in the contracting range boundary of a winter-adapted mammal. Proc. R. Soc. London Ser. B 283, 20153104 (2016).
14
D. R. Diefenbach, S. L. Rathbun, J. K. Vreeland, D. Grove, W. J. Kanapaux, Evidence for range contraction of snowshoe hare in Pennsylvania. Northeast. Nat. (Steuben) 23, 229–248 (2016).
15
S. Imperio, R. Bionda, R. Viterbi, A. Provenzale, Climate change and human disturbance can lead to local extinction of Alpine rock ptarmigan: New insight from the western Italian Alps. PLOS ONE 8, e81598 (2013).
16
S. Pedersen, M. Odden, H. C. Pedersen, Climate change induced molting mismatch? Mountain hare abundance reduced by duration of snow cover and predator abundance. Ecosphere 8, 1234 (2017).
17
E. Mayr, Animal Species and Evolution (The Belknap Press of Harvard University Press, Cambridge, MA, 1963).
18
E. R. Hall, American weasels. Univ. Kans. Publ. Mus. Nat. Hist. 4, 1–466 (1951).
19
R. M. Hansen, G. D. Bear, Winter coats of white-tailed jackrabbits in Southwestern Colorado. J. Mammal. 44, 420–422 (1963).
20
M. S. Ferreira, P. C. Alves, C. M. Callahan, J. P. Marques, L. S. Mills, J. M. Good, J. Melo-Ferreira, The transcriptional landscape of seasonal coat colour moult in the snowshoe hare. Mol. Ecol. 26, 4173–4185 (2017).
21
D. I. Våge, E. Fuglei, K. Snipstad, J. Beheim, V. M. Landsem, H. Klungland, Two cysteine substitutions in the MC1R generate the blue variant of the Arctic fox (Alopex lagopus) and prevent expression of the white winter coat. Peptides 26, 1814–1817 (2005).
22
A. Bergengren, On genetics, evolution and history of distribution of the heath-hare: A distinct population of the arctic hare, Lepus timidus. Viltrevy 6, 380–460 (1969).
23
A. Forsman, Is colour polymorphism advantageous to populations and species? Mol. Ecol. 25, 2693–2698 (2016).
24
L. Wennersten, A. Forsman, Population-level consequences of polymorphism, plasticity and randomized phenotype switching: A review of predictions. Biol. Rev. Camb. Philos. Soc. 87, 756–767 (2012).
25
T. Caro, The adaptive significance of coloration in mammals. Bioscience 55, 125–136 (2005).
26
M. Stevens, S. Merilaita, Animal camouflage: Current issues and new perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 423–427 (2009).
27
E. B. Ford, Polymorphism. Biol. Rev. Camb. Philos. Soc. 20, 73–88 (1945).
28
I. J. Saccheri, F. Rousset, P. C. Watts, P. M. Brakefield, L. M. Cook, Selection and gene flow on a diminishing cline of melanic peppered moths. Proc. Natl. Acad. Sci. U.S.A. 105, 16212–16217 (2008).
29
Materials and methods are available as supplementary materials.).
30
L. S. Mills, M. Zimova, J. Oyler, S. Running, J. T. Abatzoglou, P. M. Lukacs, Camouflage mismatch in seasonal coat color due to decreased snow duration. Proc. Natl. Acad. Sci. U.S.A. 110, 7360–7365 (2013).
31
L. Hannah, L. Flint, A. D. Syphard, M. A. Moritz, L. B. Buckley, I. M. McCullough, Fine-grain modeling of species’ response to climate change: Holdouts, stepping-stones, and microrefugia. Trends Ecol. Evol. 29, 390–397 (2014).
32
A. Hampe, A. S. Jump, Climate relicts: Past, present, future. Annu. Rev. Ecol. Evol. Syst. 42, 313–333 (2011).
33
B. Bertzky et al., Protected Plant Report 2012: Tracking progress towards global targets for protected areas (IUCN, Gland, Switzerland and UNEP-WCMC, Cambridge, UK, 2012).
34
A. Pfaff, F. Santiago-Ávila, L. Joppa, Evolving protected-area impacts in Mexico: Political shifts as suggested by impact evaluations. Forests 8, 17 (2016).
35
X. Xu, G. X. Dong, X. S. Hu, L. Miao, X. L. Zhang, D. L. Zhang, H. D. Yang, T. Y. Zhang, Z. T. Zou, T. T. Zhang, Y. Zhuang, J. Bhak, Y. S. Cho, W. T. Dai, T. J. Jiang, C. Xie, R. Li, S. J. Luo, The genetic basis of white tigers. Curr. Biol. 23, 1031–1035 (2013).
36
C. R. Camargo, E. Colares, A. M. L. Castrucci, Seasonal pelage color change: News based on a South American rodent. An. Acad. Bras. Cienc. 78, 77–86 (2006).
37
A. V. Kumar, Effects of a dynamic forest structure on vital rates, behavior and the seasonal molt of the snowshoe hare, Thesis, North Carolina State University, Raleigh, NC (2016).
38
A. J. Dietz, C. Kuenzer, S. Dech, Global SnowPack: A new set of snow cover parameters for studying status and dynamics of the planetary snow cover extent. Remote Sens. Lett. 6, 844–853 (2015).
39
D. K. Hall, G. A. Riggs, MODIS/Terra Snow Cover Daily L3 Global 500m Grid, Version 6 (Sept. 1st, 2000 - Aug. 31st, 2015). Boulder, Colorado USA. NASA National Snow and Ice Data Center Distributed Active Archive Center. Date Accessed: 24 May 24; doi: http://dx.doi.org/10.5067/MODIS/MOD10A1.006
40
R. J. Hijmans, S. E. Cameron, J. L. Parra, P. G. Jones, A. Jarvis, Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
41
M. S. O’Donnell, D. A. Ignizio, Bioclimatic predictors for supporting ecological applications in the conterminous United States. U.S. Geol. Surv. Data Ser. 691, 10 (2012).
42
D. Bates et al., Package “lme4” (2014), pp. 1–113.
43
M. Stone, An asymptotic equivalence of choice of model by cross-validation and Akaike’s criterion. J. R. Stat. Soc. B 39, 44–47 (1977).
44
R. Maggini, A. Lehmann, N. E. Zimmermann, A. Guisan, Improving generalized regression analysis for the spatial prediction of forest communities. J. Biogeogr. 33, 1729–1749 (2006).
45
L. Joppa, A. Pfaff, Reassessing the forest impacts of protection: The challenge of nonrandom location and a corrective method. Ann. N. Y. Acad. Sci. 1185, 135–149 (2010).
46
A. Nelson, K. M. Chomitz, Effectiveness of strict vs. multiple use protected areas in reducing tropical forest fires: A global analysis using matching methods. PLOS ONE 6, e22722 (2011).

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Science
Volume 359 | Issue 6379
2 March 2018

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Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Received: 1 June 2017
Accepted: 2 January 2018
Published in print: 2 March 2018

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Acknowledgments

We thank S. T. Giery, D. Emlen, and four anonymous reviewers for insightful comments on the manuscript. We also thank museum curators (table S1) and substantial sample contributions from K. Zub, K. Garrison, T. Berry, J. Dines, E. M. Fouts, K. Nicholson, D. Oehlschlager, C. Opitz, A. M. Riedel, B. Wommack, S. Lado, M. Jones, J. Ivan, J. Whittington, and A. Angerbjörn. Funding: L.S.M.: National Science Foundation Division of Environmental Biology Grant 0841884; A.V.K.: National Science Foundation Graduate Research Fellowship under grant no. DGE-1252376; P.C.A.: FLAD, Luso-American Development Foundation; M.Z.: The Department of the Interior Southeast Climate Science Center Global Change Fellowship (Cooperative Agreement No. G10AC00624); J.M.-F.: Fundação para a Ciência e a Tecnologia Grants “CHANGE” PTDC/BIA-EVF/1624/2014 (Portuguese national funds) and IF/00033/2014/CP1256/CT0005 Investigador Fundação para a Ciência e a Tecnologia (Programa Operacional Potencial Humano-Quadro de Referência Estratégica Nacional funds from European Social Fund and Ministério da Ciência, Tecnologia e Ensino Superior), and SYNTHESYS grant SE-TAF-4695 (European Union Seventh Framework Programme; agreement 226506) to access the Swedish Museum of Natural History; J.M.G.: National Science Foundation EPSCoR grant 1736249; N.L.: Russian Foundation for Basic Research (17-04-00269 A). Author contributions: L.S.M. conceived the idea, helped with analysis, and led the writing. E.B., along with A.V.K., led the data analysis, contributed conceptually, and helped with writing. M.Z. helped with data analysis, figures, writing, and contributed conceptually. D.J.R.L., J.F., B.M.D., K.H., P.C.A., J.M.G., and J.M.-F. contributed conceptually and with writing. A.D., A.V.A., N.L., and K.F. helped provide key input data. All authors read and approved the submitted manuscript. Competing interests: None declared. Data and materials availability: The data reported in the paper are available in the supplementary materials and archived in the Dryad Digital Repository at https://doi.org/10.5061/dryad.8m0p1. Global SnowPack data are available as Web Map Service at DLR (German Aerospace Center) Geoservice, https://geoservice.dlr.de.

Authors

Affiliations

L. Scott Mills*,† https://orcid.org/0000-0001-8771-509X [email protected]
Wildlife Biology Program and Office of the Vice President for Research and Creative Scholarship, University of Montana, Missoula, MT 59812, USA.
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
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Eugenia V. Bragina† https://orcid.org/0000-0001-8791-3619
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
View all articles by this author
Alexander V. Kumar https://orcid.org/0000-0003-3831-5924
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
Marketa Zimova https://orcid.org/0000-0002-8264-9879
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
Diana J. R. Lafferty https://orcid.org/0000-0001-8938-7130
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
Jennifer Feltner
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
Brandon M. Davis https://orcid.org/0000-0003-2013-7875
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
Klaus Hackländer https://orcid.org/0000-0002-6774-435X
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
Institute of Wildlife Biology and Game Management, BOKU, University of Natural Resources and Life Sciences, Vienna, Austria.
View all articles by this author
Paulo C. Alves https://orcid.org/0000-0003-4797-0939
Wildlife Biology Program, University of Montana, Missoula, MT 59812, USA.
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.
Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre 4169-007 Porto, Portugal.
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Jeffrey M. Good https://orcid.org/0000-0003-0707-5374
Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA.
View all articles by this author
José Melo-Ferreira https://orcid.org/0000-0003-4473-1908
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.
Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre 4169-007 Porto, Portugal.
View all articles by this author
Andreas Dietz
German Aerospace Center, Earth Observation Center, German Remote Sensing Data Center, Oberpfaffenhofen, Wessling 82234, Germany.
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Alexei V. Abramov https://orcid.org/0000-0001-9709-4469
Zoological Institute, Russian Academy of Science, Saint Petersburg 199034, Russia.
View all articles by this author
Natalia Lopatina https://orcid.org/0000-0003-4660-0936
Institute of Systematics and Ecology of Animals SB RAS, Novosibirsk, 630091, Russia.
View all articles by this author
Kairsten Fay
Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.
View all articles by this author

Funding Information

Notes

*Corresponding author. Email: [email protected]
†
These authors contributed equally to this work.

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