Page 102 - Science

RESEARCH

ADAPTATION ly, color polymorphisms have served as powerful
models demonstrating evolution in nature, includ-
Winter color polymorphisms identify ing iconic examples of evolutionary response to
anthropogenic stressors (25–28). For the seasonal
coat color trait, selection is expected to act on all
global hot spots for evolutionary winter color morphs based on local snow dura-
tion, but evolutionary rescue to changing climate
rescue from climate change shouldbe enhanced bypolymorphicregions where
both brown and white winter morphs co-occur.
Here, we use a hierarchical approach across
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L. Scott Mills, 1,2 *† Eugenia V. Bragina, † Alexander V. Kumar, 2,3 Marketa Zimova, 2,3 organismal scales (individual, population, and spe-
Diana J. R. Lafferty, 2,3 Jennifer Feltner, 2,3 Brandon M. Davis, 2,3 Klaus Hackländer, 2,4 cies) to spatially map geographic clines in winter
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Paulo C. Alves, 3,5,6 Jeffrey M. Good, José Melo-Ferreira, 5,6 Andreas Dietz, 8 coat color against local climate variables (29). We
collated georeferenced descriptions of winter coat
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Alexei V. Abramov, Natalia Lopatina, 10 Kairsten Fay 2
color from 2713 specimens spanning 60 countries
across species ranges, with data sources including
Maintenance of biodiversity in a rapidly changing climate will depend on the efficacy of
published accounts and specimens at 26 muse-
evolutionary rescue, whereby population declines due to abrupt environmental change are
ums globally (table S1). From these georeferenced
reversed by shifts in genetically driven adaptive traits. However, a lack of traits known to be under
winter color morph samples, we built predictive
direct selection by anthropogenic climate change has limited the incorporation of evolutionary
models of winter color phenotypes across geo-
processes into global conservation efforts. In 21 vertebrate species, some individuals undergo a
graphic ranges for eight mammal species that span
seasonal color molt from summer brown to winter white as camouflage against snow, whereas
trophic levels: four hare species and four carni-
other individuals remain brown. Seasonal snow duration is decreasing globally, and fitness is
vore species (three weasels and Arctic fox).
lower for winter white animals on snowless backgrounds. Based on 2713 georeferenced samples Theresponse variablefor ourglobalgeneral-
of known winter coat color—from eight species across trophic levels—we identify environmentally ized mixed model was the probability of an indi- Downloaded from
driven clinal gradients in winter coat color, including polymorphic zones where winter brown vidual having a winter white coat, with species as
and white morphs co-occur.These polymorphic zones, underrepresented by existing global a random effect and fixed effects including cli-
protected area networks, indicate hot spots for evolutionary rescue in a changing climate.
mate and landscape-level covariates (table S2). As
expected for a trait under selection for crypsis
he importance of evolution in fostering the mammal species undergo photoperiod-induced against snow or bare ground, the most important
persistence of species facing rapid environ- seasonal coat color molts from brown to white covariates emerging from the global model were
mental change is a fundamental tenet of in some portions of their range to maintain cryp- snow-cover duration and two climate variables
biology that underlies the modern field of sis against seasonal snow presence or absence affecting snow seasonality and transience. The
T conservation biology (1–3). Despite the cen- (Table 1). This seasonal phenological trait is con- probability of being white in winter (as opposed http://science.sciencemag.org/
tral role of evolution for maintaining biodiversity, fronting decreased seasonal snow cover dura- to brown) increased positively with snow duration
criteria to facilitate adaptation by wild species tion, one of the most persistent and widespread and with seasonality (ranges of mean monthly
remain largely absent from conservation planning signals of climate change (10, 11). Field studiesshow temperatures), and negatively with isothermality
(4, 5). This is a particularly acute omission in a that winter white animals mismatched against (an index of snow transience).
rapidly changing climate (6, 7) where evolutionary snowless ground suffer high fitness costs due to Using the three environmental covariates iden-
rescue may reverse population declines via adap- increased predator-caused mortality, which in tified in the best-fitting model, we created for
tive evolutionary change in phenotypes (2, 8, 9). the absence of evolutionary shifts would result each of the eight species a predictive range-wide
As a first step to demonstrate how evolution- in substantial population declines (12). In fact, map that assigned to each pixel a probability of on March 1, 2018
ary rescue might enter conservation planning for coat color mismatch against decreased snow du- an individual being white in winter (Fig. 1 and
climate change, we describe a fitness-relevant trait ration mayhavealready contributedtorange figs. S1 to S8). Based on fivefold cross validation,
that exhibits clines of locally adapted morphs contractions for several species (13–16). models fit georeferenced winter color morph
shaped directly by climate. At least 21 bird and Although the seasonal brown-white-brown data well (29). Across species, clinal gradients in
color trait is a classic polyphenism—whereby winter color follow expected environmental gra-
multiple morphs are produced by a single indi- dients based on snow duration and ephemeral-
1 Wildlife Biology Program and Office of the Vice President for vidual (17)—individuals in some populations molt ity: Winter white morphs were more likely in
Research and Creative Scholarship, University of Montana, to brown winter coats, thereby not undergoing regions with more persistent snowpack that
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Missoula, MT 59812, USA. Fisheries, Wildlife, and Conservation the circannual color change. This intraspecific tended to be more northern, higher elevation,
Biology Program, Department of Forestry and Environmental variation results in monomorphic winter white and less maritime (Fig. 1). These results suggest
Resources, North Carolina State University, Raleigh, NC 27695, and brown populations but also in polymorphic that strong natural selection for camouflage
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USA. Wildlife Biology Program, University of Montana,
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Missoula, MT 59812, USA. Institute of Wildlife Biology and populations that include sympatric winter white against varying snow duration underlies pheno-
Game Management, BOKU, University of Natural Resources and and brown color morphs. Importantly, this phe- typic variation in winter color morphs across en-
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Life Sciences, Vienna, Austria. CIBIO, Centro de Investigação notypic variation is genetically determined: Latitu- vironmental gradients.
em Biodiversidade e Recursos Genéticos, InBIO Laboratório dinal transplants, common garden, and breeding To identify hot spots that foster evolutionary
Associado, Universidade do Porto, Campus Agrário de Vairão,
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4485-661 Vairão, Portugal. Departamento de Biologia, experiments with several seasonal color molting rescue, we converted the continuous probabili-
Faculdade de Ciências da Universidade do Porto, Rua do species have consistently showed minimal plas- ties of individuals being winter white (versus brown)
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Campo Alegre 4169-007 Porto, Portugal. Division of Biological ticity in the expression of winter phenotype and into polymorphic zones, using both a narrow
Sciences, University of Montana, Missoula, MT 59812, USA.
8 German Aerospace Center, Earth Observation Center, German instead suggested a simple genetic basis involv- (40%<Probability[winterwhite]<60%)andbroad
Remote Sensing Data Center, Oberpfaffenhofen, Wessling ing one or a few major loci [e.g., (18–22)]. (20% < Probability [winter white] < 80%) criteria.
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82234, Germany. Zoological Institute, Russian Academy of The enhanced standing phenotypic variation Depending on the species and criteria, polymor-
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Science, Saint Petersburg 199034, Russia. Institute of fostered by genetically based polymorphisms have phic zones comprised 1 to 57% of a species’ range
Systematics and Ecology of Animals SB RAS, Novosibirsk, long been linked to individual fitness and to po- (table S4). The species with the most widespread
630091, Russia.
*Corresponding author. Email: scott.mills@umontana.edu tential for evolution to rescue populations from polymorphic zones (for narrow/broad criteria)
†These authors contributed equally to this work. abrupt environmental change (23, 24). Specifical- are arctic fox (10%/57%), white-tailed jackrabbit
Mills et al., Science 359, 1033–1036 (2018) 2 March 2018 1of4