ADAPTIVE POTENTIAL TO CAMOUFLAGE MISMATCH: PLASTIC AND EVOLUTIONARY RESPONSES TO A CLIMATE CHANGE STRESSOR

Animals that occupy temperate and polar regions have specialized traits that help them survive in harsh, highly seasonal environments. One particularly important adaptation is seasonal coat colour (SCC) moulting. Over 20 species of birds and mammals distributed across the northern hemisphere undergo complete, biannual colour change from brown in the summer to completely white in the winter. But as climate change decreases duration of snow cover, seasonally winter white species (including the snowshoe hare Lepus americanus, Arctic fox Vulpes lagopus and willow ptarmigan Lagopus lagopus) become highly contrasted against dark snowless backgrounds. The negative consequences of camouflage mismatch and adaptive potential is of high interest for conservation. Here we provide the first comprehensive review across birds and mammals of the adaptive value and mechanisms underpinning SCC moulting. We found that across species, the main function of SCC moults is seasonal camouflage against snow, and photoperiod is the main driver of the moult phenology. Next, although many underlying mechanisms remain unclear, mammalian species share similarities in some aspects of hair growth, neuroendocrine control, and the effects of intrinsic and extrinsic factors on moult phenology. The underlying basis of SCC moults in birds is less understood and differs from mammals in several aspects. Lastly, our synthesis suggests that due to limited plasticity in SCC moulting, evolutionary adaptation will be necessary to mediate future camouflage mismatch and a detailed understanding of the SCC moulting in all species will be needed to manage populations effectively under climate change

Camouflage mismatch in seasonal coat color due to decreased snow duration: Will snowshoe hares keep up with climate change?

As wild species face anthropogenic stressors, they will either adapt, shift their geographic range, or decline, perhaps towards extinction. The relative scope of these responses has not been well studied, especially for climate change where geographic range shifts and population declines have been widely discussed but the potential for adaptation mostly ignored. Adaptation to anthropogenic stressors can occur through phenotypic plasticity and/or evolution. My thesis first establishes, based on field studies of wild snowshoe hares, a novel and high-profile stressor directly linked to climate change. The stressor arises from a decrease in snow duration due to climate change, which causes seasonal coat color molt of individual hares to become mismatched with their background. The immediate adaptive solution to this form of camouflage mismatch is phenotypic plasticity, either in phenology of seasonal color molts or in behaviors that reduce mismatch or its consequences. Based on nearly 200 snowshoe hares across a wide range of snow conditions and two study sites in Montana, USA that differed in elevation and climate, I found minimal plasticity in response to mismatch between coat color and background. I found that molt phenology varied between study sites, likely due to differences in photoperiod and climate, but was largely fixed within study sites where seasonal changes in phenology were limited across years of very different snow duration. Hares exhibited some plasticity in the rate of the spring molt in response to immediate snow conditions but temperature or snow cover were not strong modifiers of the white-to-brown molt phenology. I also found no evidence that individual hares modify their behavior in response to color mismatch. Hiding and fleeing behaviors and immediate microsite preference of hares were more affected by variables related to season, site, and concealment, than by color mismatch. Although hares do not appear to be responding to camouflage mismatch with behavioral plasticity, adaptation could also occur through evolutionary changes facilitated by natural selection. We found that the raw material for natural selection to act on does exist in our populations in the form of individual variation in coat color phenology and consequently in color mismatch. We also found high fitness costs of coat color mismatch, with hares suffering 3 to 7% lower weekly survival rates when mismatched against their background. Coupling these fitness costs to local estimates of increased seasonal color mismatch as snow duration decreases in the future, we predict that annual hare survival will decline up to 12% by mid- and 24% by late century. Such changes in survival are sufficient to cause increasing hare populations to decline strongly towards extinction, with annual population geometric growth rate decreasing by 11% (24%) by mid (late) century. We conclude that plasticity in molt phenology and behaviors in snowshoe hares is insufficient for adaptation to camouflage mismatch, and that potential adaptive responses to future climate change will have to be facilitated by natural selection. These results form the basis for future work to evaluate whether evolution by natural selection can operate fast enough to prevent decline of this species

Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage

As duration of snow cover decreases owing to climate change, species undergoing seasonal colour moults can become colour mismatched with their background. The immediate adaptive solution to this mismatch is phenotypic plasticity, either in phenology of seasonal colour moults or in behaviours that reduce mismatch or its consequences. We observed nearly 200 snowshoe hares across a wide range of snow conditions and two study sites in Montana, USA, and found minimal plasticity in response to mismatch between coat colour and background. We found that moult phenology varied between study sites, likely due to differences in photoperiod and climate, but was largely fixed within study sites with only minimal plasticity to snow conditions during the spring white-to-brown moult. We also found no evidence that hares modify their behaviour in response to colour mismatch. Hiding and fleeing behaviours and resting spot preference of hares were more affected by variables related to season, site and concealment by vegetation, than by colour mismatch. We conclude that plasticity in moult phenology and behaviours in snowshoe hares is insufficient for adaptation to camouflage mismatch, suggesting that any future adaptation to climate change will require natural selection on moult phenology or behaviour

Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world?

Animals that occupy temperate and polar regions have specialized traits that help them survive in harsh, highly seasonal environments. One particularly important adaptation is seasonal coat colour (SCC) moulting. Over 20 species of birds and mammals distributed across the northern hemisphere undergo complete, biannual colour change from brown in the summer to completely white in the winter. But as climate change decreases duration of snow cover, seasonally winter white species (including the snowshoe hare Lepus americanus, Arctic fox Vulpes lagopus and willow ptarmigan Lagopus lagopus) become highly contrasted against dark snowless backgrounds. The negative consequences of camouflage mismatch and adaptive potential is of high interest for conservation. Here we provide the first comprehensive review across birds and mammals of the adaptive value and mechanisms underpinning SCC moulting. We found that across species, the main function of SCC moults is seasonal camouflage against snow, and photoperiod is the main driver of the moult phenology. Next, although many underlying mechanisms remain unclear, mammalian species share similarities in some aspects of hair growth, neuroendocrine control, and the effects of intrinsic and extrinsic factors on moult phenology. The underlying basis of SCC moults in birds is less understood and differs from mammals in several aspects. Lastly, our synthesis suggests that due to limited plasticity in SCC moulting, evolutionary adaptation will be necessary to mediate future camouflage mismatch and a detailed understanding of the SCC moulting will be needed to manage populations effectively under climate change

Shared morphological consequences of global warming in North American migratory birds

Increasing temperatures associated with climate change are predicted to cause reductions in body size, a key determinant of animal physiology and ecology. Using a four‐decade specimen series of 70 716 individuals of 52 North American migratory bird species, we demonstrate that increasing annual summer temperature over the 40‐year period predicts consistent reductions in body size across these diverse taxa. Concurrently, wing length – an index of body shape that impacts numerous aspects of avian ecology and behaviour – has consistently increased across species. Our findings suggest that warming‐induced body size reduction is a general response to climate change, and reveal a similarly consistent and unexpected shift in body shape. We hypothesise that increasing wing length represents a compensatory adaptation to maintain migration as reductions in body size have increased the metabolic cost of flight. An improved understanding of warming‐induced morphological changes is important for predicting biotic responses to global change.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/153188/1/ele13434-sup-0001-Supinfo.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/153188/2/ele13434.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/153188/3/ele13434_am.pd

A Great Escape : resource availability and density-dependence shape population dynamics along trailing range edges

This research was funded by the Northeast Climate Adaptation Science Center, which is managed by the USGS National Climate Adaptation Science Center. Additional funding was provided by 1) a CFDA grant (15.678) administered by the USFWS via a Cooperative Agreement Award (no. F16AC00435) to the University of Massachusetts (UMass); 2) a Challenge Cost Share Agreement (no. 14-CS-11092200-019) between the USFS and NHFG; 3) a Dissertation Fieldwork Grant awarded to APKS by the UMass Graduate School, 4) generous support from backers of an Experiment award to APKS and MZ (DOI: 10.18258/10737) and 5) a National Science Foundation grant DEB-1907022 to LSM.Populations along geographical range limits are often exposed to unsuitable climate and low resource availability relative to core populations. As such, there has been a renewed focus on understanding the factors that determine range limits to better predict how species will respond to global change. Using recent theory on range limits and classical understanding of density dependence, we evaluated the influence of resource availability on the snowshoe hare Lepus americanus along its trailing range edge. We estimated variation in population density, habitat use, survival, and parasite loads to test the Great Escape Hypothesis (GEH), i.e. that density dependence determines, in part, a species' persistence along trailing edges. We found that variability in resource availability affected density and population fluctuations and led to trade-offs in survival for snowshoe hare populations in the northeastern USA. Hares living in resource-limited environments had lower and less variable population density, yet higher survival and lower parasitism compared to populations living in resource-rich environments. We suggest that density-dependent dynamics, elicited by resource availability, provide hares a unique survival advantage and partly explain persistence along their trailing edge. We hypothesize that this low-density escape from predation and parasitism occurs for other prey species along trailing edges, but the extent to which it occurs is likely conditional on the quality of matrix habitat. Our work indicates that biotic factors play an important role in shaping species' trailing edges and more detailed examination of non-climatic factors is warranted to better inform conservation and management decisions.Publisher PDFPeer reviewe

Museomics Dissects the Genetic Basis for Adaptive Seasonal Coloration in the Least Weasel

Dissecting the link between genetic variation and adaptive phenotypes provides outstanding opportunities to understand fundamental evolutionary processes. Here, we use a museomics approach to investigate the genetic basis and evolution of winter coat coloration morphs in least weasels (Mustela nivalis), a repeated adaptation for camouflage in mammals with seasonal pelage color moults across regions with varying winter snow. Whole-genome sequence data were obtained from biological collections and mapped onto a newly assembled reference genome for the species. Sampling represented two replicate transition zones between nivalis and vulgaris coloration morphs in Europe, which typically develop white or brown winter coats, respectively. Population analyses showed that the morph distribution across transition zones is not a by-product of historical structure. Association scans linked a 200-kb genomic region to coloration morph, which was validated by genotyping museum specimens from intermorph experimental crosses. Genotyping the wild populations narrowed down the association to pigmentation gene MC1R and pinpointed a candidate amino acid change cosegregating with coloration morph. This polymorphism replaces an ancestral leucine residue by lysine at the start of the first extracellular loop of the protein in the vulgaris morph. A selective sweep signature overlapped the association region in vulgaris, suggesting that past adaptation favored winter-brown morphs and can anchor future adaptive responses to decreasing winter snow. Using biological collections as valuable resources to study natural adaptations, our study showed a new evolutionary route generating winter color variation in mammals and that seasonal camouflage can be modulated by changes at single key genes

SNAPSHOT USA 2019 : a coordinated national camera trap survey of the United States

This article is protected by copyright. All rights reserved.With the accelerating pace of global change, it is imperative that we obtain rapid inventories of the status and distribution of wildlife for ecological inferences and conservation planning. To address this challenge, we launched the SNAPSHOT USA project, a collaborative survey of terrestrial wildlife populations using camera traps across the United States. For our first annual survey, we compiled data across all 50 states during a 14-week period (17 August - 24 November of 2019). We sampled wildlife at 1509 camera trap sites from 110 camera trap arrays covering 12 different ecoregions across four development zones. This effort resulted in 166,036 unique detections of 83 species of mammals and 17 species of birds. All images were processed through the Smithsonian's eMammal camera trap data repository and included an expert review phase to ensure taxonomic accuracy of data, resulting in each picture being reviewed at least twice. The results represent a timely and standardized camera trap survey of the USA. All of the 2019 survey data are made available herein. We are currently repeating surveys in fall 2020, opening up the opportunity to other institutions and cooperators to expand coverage of all the urban-wild gradients and ecophysiographic regions of the country. Future data will be available as the database is updated at eMammal.si.edu/snapshot-usa, as well as future data paper submissions. These data will be useful for local and macroecological research including the examination of community assembly, effects of environmental and anthropogenic landscape variables, effects of fragmentation and extinction debt dynamics, as well as species-specific population dynamics and conservation action plans. There are no copyright restrictions; please cite this paper when using the data for publication.Publisher PDFPeer reviewe

Widespread shifts in bird migration phenology are decoupled from parallel shifts in morphology

Advancements in phenology and changes in morphology, including body size reductions, are among the most commonly described responses to globally warming temperatures. Although these dynamics are routinely explored independently, the relationships among them and how their interactions facilitate or constrain adaptation to climate change are poorly understood.In migratory species, advancing phenology may impose selection on morphological traits to increase migration speed. Advancing spring phenology might also expose species to cooler temperatures during the breeding season, potentially mitigating the effect of a warming global environment on body size.We use a dataset of birds that died after colliding with buildings in Chicago, IL to test whether changes in migration phenology are related to documented declines in body size and increases in wing length in 52 North American migratory bird species between 1978 and 2016. For each species, we estimate temporal trends in morphology and changes in the timing of migration. We then test for associations between species‐specific rates of phenological and morphological changes while assessing the potential effects of migratory distance and breeding latitude.We show that spring migration through Chicago has advanced while the timing of fall migration has broadened as a result of early fall migrants advancing their migrations and late migrants delaying their migrations. Within species, we found that longer wing length was linked to earlier spring migration within years. However, we found no evidence that rates of phenological change across years, or migratory distance and breeding latitude, are predictive of rates of concurrent changes in morphological traits.These findings suggest that biotic responses to climate change are highly multidimensional and the extent to which those responses interact and influence adaptation to climate change requires careful examination.This study represents a unique empirical assessment of a presumed connection between shifting phenology and morphology using >70,000 museum specimens of 52 species of migratory birds collected during 1978–2016. The authors discovery that these axes of adaptation are apparently decoupled has broad implications for predicting future responses to climate change.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/170852/1/jane13543.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/170852/2/jane13543_am.pd