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The genetic basis of adaptive traits has rarely been used to predict future vulnerability of populations to climate change. We show that light versus dark seasonal pelage in white-tailed jackrabbits (Lepus townsendii) tracks snow cover and is primarily determined by genetic variation at endothelin receptor type B (EDNRB), corin serine peptidase (CORIN), and agouti signaling protein (ASIP). Winter color variation was associated with deeply divergent alleles at these genes, reflecting selection on both ancestral and introgressed variation. Forecasted reductions in snow cover are likely to induce widespread camouflage mismatch. However, simulated populations with variation for darker winter pelage are predicted to adapt rapidly, providing a trait-based genetic framework to facilitate evolutionary rescue. These discoveries demonstrate how the genetic basis of climate change adaptation can inform conservation.
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Aclimatación , Mimetismo Biológico , Cambio Climático , Liebres , Animales , Aclimatación/genética , Liebres/genética , Liebres/fisiología , Estaciones del Año , Mimetismo Biológico/genética , Receptor de Endotelina B/genética , Variación Genética , Serina Endopeptidasas/genética , Proteína de Señalización Agouti/genéticaRESUMEN
Species that seasonally moult from brown to white to match snowy backgrounds become conspicuous and experience increased predation risk as snow cover duration declines. Long-term adaptation to camouflage mismatch in a changing climate might occur through phenotypic plasticity in colour moult phenology and or evolutionary shifts in moult rate or timing. Also, adaptation may include evolutionary shifts towards winter brown phenotypes that forgo the winter white moult. Most studies of these processes have occurred in winter white populations, with little attention to polymorphic populations with sympatric winter brown and winter white morphs. Here, we used remote camera traps to record moult phenology and mismatch in two polymorphic populations of Arctic foxes in Sweden over 2 years. We found that the colder, more northern population moulted earlier in the autumn and later in the spring. Next, foxes moulted earlier in the autumn and later in the spring during colder and snowier years. Finally, white foxes experienced relatively low camouflage mismatch while blue foxes were mismatched against snowy backgrounds most of the autumn through the spring. Because the brown-on-white mismatch imposes no evident costs, we predict that as snow duration decreases, increasing blue morph frequencies might help facilitate species persistence.
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Cambio Climático , Zorros , Animales , Color , Muda , Nieve , Estaciones del Año , Regiones ÁrticasRESUMEN
Many ecological processes are profoundly influenced by abiotic factors, such as temperature and snow. However, despite strong evidence linking shifts in these ecological processes to corresponding shifts in abiotic factors driven by climate change, the mechanisms connecting population size to season-specific climate drivers are little understood. Using a 21-year dataset and a Bayesian state space model, we identified biologically informed seasonal climate covariates that influenced densities of snowshoe hares (Lepus americanus), a cold-adapted boreal herbivore. We found that snow and temperature had strong but conflicting season-dependent effects. Reduced snow duration in spring and fall and warmer summers were associated with lowered hare density, whereas warmer winters were associated with increased density. When modeled simultaneously and under two climate change scenarios, the negative effects of reduced fall and spring snow duration and warmer summers overwhelm the positive effect of warmer winters, producing projected population declines. Ultimately, the contrasting population-level impacts of climate change across seasons emphasize the critical need to examine the entire annual climate cycle to understand potential long-term population consequences of climate change.
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Cambio Climático , Liebres , Animales , Teorema de Bayes , Estaciones del Año , NieveRESUMEN
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.
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Mustelidae , Pigmentación , Animales , Mamíferos , Mustelidae/fisiología , Fenotipo , Pigmentación/genética , Estaciones del AñoRESUMEN
Hybridization may often be an important source of adaptive variation, but the extent and long-term impacts of introgression have seldom been evaluated in the phylogenetic context of a radiation. Hares (Lepus) represent a widespread mammalian radiation of 32 extant species characterized by striking ecological adaptations and recurrent admixture. To understand the relevance of introgressive hybridization during the diversification of Lepus, we analyzed whole exome sequences (61.7 Mb) from 15 species of hares (1-4 individuals per species), spanning the global distribution of the genus, and two outgroups. We used a coalescent framework to infer species relationships and divergence times, despite extensive genealogical discordance. We found high levels of allele sharing among species and show that this reflects extensive incomplete lineage sorting and temporally layered hybridization. Our results revealed recurrent introgression at all stages along the Lepus radiation, including recent gene flow between extant species since the last glacial maximum but also pervasive ancient introgression occurring since near the origin of the hare lineages. We show that ancient hybridization between northern hemisphere species has resulted in shared variation of potential adaptive relevance to highly seasonal environments, including genes involved in circadian rhythm regulation, pigmentation, and thermoregulation. Our results illustrate how the genetic legacy of ancestral hybridization may persist across a radiation, leaving a long-lasting signature of shared genetic variation that may contribute to adaptation. [Adaptation; ancient introgression; hybridization; Lepus; phylogenomics.].
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Liebres , Animales , ADN Mitocondrial , Flujo Génico , Liebres/genética , Humanos , Hibridación Genética , Filogenia , PigmentaciónRESUMEN
Understanding whether organisms will be able to adapt to human-induced stressors currently endangering their existence is an urgent priority. Globally, multiple species moult from a dark summer to white winter coat to maintain camouflage against snowy landscapes. Decreasing snow cover duration owing to climate change is increasing mismatch in seasonal camouflage. To directly test for adaptive responses to recent changes in snow cover, we repeated historical (1950s) field studies of moult phenology in mountain hares (Lepus timidus) in Scotland. We found little evidence that population moult phenology has shifted to align seasonal coat colour with shorter snow seasons, or that phenotypic plasticity prevented increases in camouflage mismatch. The lack of responses resulted in 35 additional days of mismatch between 1950 and 2016. We emphasize the potential role of weak directional selection pressure and low genetic variability in shaping the scope for adaptive responses to anthropogenic stressors.
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Adaptación Fisiológica , Liebres , Fenotipo , Pigmentos Biológicos , Animales , Cambio Climático , Color , Humanos , Muda , Estaciones del Año , NieveRESUMEN
Canine distemper virus (CDV) is a multi-host pathogen with variable clinical outcomes of infection across and within species. We used whole-genome sequencing (WGS) to search for viral markers correlated with clinical distemper in African lions. To identify candidate markers, we first documented single-nucleotide polymorphisms (SNPs) differentiating CDV strains associated with different clinical outcomes in lions in East Africa. We then conducted evolutionary analyses on WGS from all global CDV lineages to identify loci subject to selection. SNPs that both differentiated East African strains and were under selection were mapped to a phylogenetic tree representing global CDV diversity to assess if candidate markers correlated with documented outbreaks of clinical distemper in lions (n = 3). Of 54 SNPs differentiating East African strains, ten were under positive or episodic diversifying selection and 20 occurred in the clinical strain despite strong purifying selection at those loci. Candidate markers were in functional domains of the RNP complex (n = 19), the matrix protein (n = 4), on CDV glycoproteins (n = 5), and on the V protein (n = 1). We found mutations at two loci in common between sequences from three CDV outbreaks of clinical distemper in African lions; one in the signaling lymphocytic activation molecule receptor (SLAM)-binding region of the hemagglutinin protein and another in the catalytic center of phosphodiester bond formation on the large polymerase protein. These results suggest convergent evolution at these sites may have a functional role in clinical distemper outbreaks in African lions and uncover potential novel barriers to pathogenicity in this species.
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AbstractAdaptation is central to population persistence in the face of environmental change, yet we seldom precisely understand the origin and spread of adaptive variation in natural populations. Snowshoe hares (Lepus americanus) along the Pacific Northwest coast have evolved brown winter camouflage through positive selection on recessive variation at the Agouti pigmentation gene introgressed from black-tailed jackrabbits (Lepus californicus). Here, we combine new and published whole-genome and exome sequences with targeted genotyping of Agouti to investigate the evolutionary history of local seasonal camouflage adaptation in the Pacific Northwest. We find evidence of significantly elevated inbreeding and mutational load in coastal winter-brown hares, consistent with a recent range expansion into temperate coastal environments that incurred indirect fitness costs. The genome-wide distribution of introgression tract lengths supports a pulse of hybridization near the end of the last glacial maximum, which may have facilitated range expansion via introgression of winter-brown camouflage variation. However, signatures of a selective sweep at Agouti indicate a much more recent spread of winter-brown camouflage. Through simulations, we show that the delay between the hybrid origin and subsequent selective sweep of the recessive winter-brown allele can be largely attributed to the limits of natural selection imposed by simple allelic dominance. We argue that while hybridization during periods of environmental change may provide a critical reservoir of adaptive variation at range edges, the probability and pace of local adaptation will strongly depend on population demography and the genetic architecture of introgressed variation.
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Adaptación Biológica , Liebres/genética , Hibridación Genética , Pigmentación/genética , Selección Genética , Animales , Colombia Británica , Cambio Climático , Color , Montana , Oregon , Estaciones del Año , WashingtónRESUMEN
Global reduction in snow cover duration is one of the most consistent and widespread climate change outcomes. Declining snow duration has severe negative consequences for diverse taxa including seasonally color molting species, which rely on snow for camouflage. However, phenotypic plasticity may facilitate adaptation to reduced snow duration. Plastic responses could occur in the color molt phenology or through behavior that minimizes coat color mismatch or its consequences. We quantified molt phenology of 200 wild snowshoe hares (Lepus americanus), and measured microhabitat choice and local snow cover. Similar to other studies, we found that hares did not show behavioral plasticity to minimize coat color mismatch via background matching; instead they preferred colder, snow free areas regardless of their coat color. Furthermore, hares did not behaviorally mitigate the negative consequences of mismatch by choosing resting sites with denser vegetation cover when mismatched. Importantly, we demonstrated plasticity in the initiation and the rate of the molt and established the direct effect of snow on molt phenology; greater snow cover was associated with whiter hares and this association was not due to whiter hares preferring snowier areas. However, despite the observed snow-mediated plasticity in molt phenology, camouflage mismatch with white hares on brown snowless ground persisted and was more frequent during early snowmelt. Thus, we find no evidence that phenotypic plasticity in snowshoe hares is sufficient to facilitate adaptive rescue to camouflage mismatch under climate change.
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Liebres , Nieve , Animales , Cambio Climático , Muda , Estaciones del AñoRESUMEN
The outcome of pathogen spillover from a reservoir to a novel host population can range from a "dead-end" when there is no onward transmission in the recipient population, to epidemic spread and even establishment in new hosts. Understanding the evolutionary epidemiology of spillover events leading to discrete outcomes in novel hosts is key to predicting risk and can lead to a better understanding of the mechanisms of emergence. Here we use a Bayesian phylodynamic approach to examine cross-species transmission and evolutionary dynamics during a canine distemper virus (CDV) spillover event causing clinical disease and population decline in an African lion population (Panthera leo) in the Serengeti Ecological Region between 1993 and 1994. Using 21 near-complete viral genomes from four species we found that this large-scale outbreak was likely ignited by a single cross-species spillover event from a canid reservoir to noncanid hosts <1 year before disease detection and explosive spread of CDV in lions. Cross-species transmission from other noncanid species probably fuelled the high prevalence of CDV across spatially structured lion prides. Multiple lines of evidence suggest that spotted hyenas (Crocuta crocuta) could have acted as the proximate source of CDV exposure in lions. We report 13 nucleotide substitutions segregating CDV strains found in canids and noncanids. Our results are consistent with the hypothesis that virus evolution played a role in CDV emergence in noncanid hosts following spillover during the outbreak, suggest that host barriers to clinical infection can limit outcomes of CDV spillover in novel host species.
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Virus del Moquillo Canino , Moquillo , Leones , Animales , Animales Salvajes , Teorema de Bayes , Moquillo/epidemiología , Virus del Moquillo Canino/genética , Parques RecreativosRESUMEN
Determining how different populations adapt to similar environments is fundamental to understanding the limits of adaptation under changing environments. Snowshoe hares (Lepus americanus) typically molt into white winter coats to remain camouflaged against snow. In some warmer climates, hares have evolved brown winter camouflage-an adaptation that may spread in response to climate change. We used extensive range-wide genomic data to (1) resolve broad patterns of population structure and gene flow and (2) investigate the factors shaping the origins and distribution of winter-brown camouflage variation. In coastal Pacific Northwest (PNW) populations, winter-brown camouflage is known to be determined by a recessive haplotype at the Agouti pigmentation gene. Our phylogeographic analyses revealed deep structure and limited gene flow between PNW and more northern Boreal populations, where winter-brown camouflage is rare along the range edge. Genome sequencing of a winter-brown snowshoe hare from Alaska shows that it lacks the winter-brown PNW haplotype, reflecting a history of convergent phenotypic evolution. However, the PNW haplotype does occur at low frequency in a winter-white population from Montana, consistent with the spread of a locally deleterious recessive variant that is masked from selection when rare. Simulations of this population further show that this masking effect would greatly slow the selective increase of the winter-brown Agouti allele should it suddenly become beneficial (e.g., owing to dramatic declines in snow cover). Our findings underscore how allelic dominance can shape the geographic extent and rate of convergent adaptation in response to rapidly changing environments.
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Adaptación Biológica , Mimetismo Biológico , Cambio Climático , Liebres/fisiología , Pigmentación , Nieve , Distribución Animal , Animales , Canadá , Color , Estaciones del Año , Estados UnidosRESUMEN
Color molts from summer brown to winter white coats have evolved in several species to maintain camouflage year-round in environments with seasonal snow. Despite the eco-evolutionary relevance of this key phenological adaptation, its molecular regulation has only recently begun to be addressed. Here, we analyze skin transcription changes during the autumn molt of the mountain hare (Lepus timidus) and integrate the results with an established model of gene regulation across the spring molt of the closely related snowshoe hare (L. americanus). We quantified differences in gene expression among three stages of molt progression-"brown" (early molt), "intermediate," and "white" (late molt). We found 632 differentially expressed genes, with a major pulse of expression early in the molt, followed by a milder one in late molt. The functional makeup of differentially expressed genes anchored the sampled molt stages to the developmental timeline of the hair growth cycle, associating anagen to early molt and the transition to catagen to late molt. The progression of color change was characterized by differential expression of genes involved in pigmentation, circadian, and behavioral regulation. We found significant overlap between differentially expressed genes across the seasonal molts of mountain and snowshoe hares, particularly at molt onset, suggesting conservatism of gene regulation across species and seasons. However, some discrepancies suggest seasonal differences in melanocyte differentiation and the integration of nutritional cues. Our established regulatory model of seasonal coat color molt provides an important mechanistic context to study the functional architecture and evolution of this crucial seasonal adaptation.
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Glucocorticoids and glucocorticoid metabolites are increasingly used to index physiological stress in wildlife. Although feces is often abundant and can be collected noninvasively, exposure to biotic and abiotic elements may influence fecal glucocorticoid metabolite (FGM) concentrations, leading to inaccurate conclusions regarding wildlife physiological stress. Using captive snowshoe hares (Lepus americanus) and simulated environmental conditions, we evaluated how different realistic field conditions and temporal sampling constraints might influence FGM concentrations using an 11-oxoetiocholanolone-enzyme immunoassay. We quantified how fecal pellet age (i.e., 0-6 days), variable summer temperatures, and precipitation affected FGM concentrations. Fecal pellet age had a strong effect on FGM concentrations (ßAge = 0.395, s.d. = 0.085; ß2Age = -0.061, s.d. = 0.012), which were lowest at the beginning and end of our exposure period (e.g., meanday6 = 37.7 ng/mg) and typically highest in the middle (meanday3 = 51.8 ng/mg). The effect of fecal pellet age on FGM concentrations varied across treatments with warm-dry and cool-wet conditions resulting in more variable FGM concentrations relative to control samples. Given the confounding effects of exposure and environmental conditions, if fresh fecal pellet collection is not an option, we encourage researchers to develop a temporally consistent sampling protocol to ensure all samples are exposed to similar environmental conditions.
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Exposición a Riesgos Ambientales , Liebres/fisiología , Estrés Fisiológico , Animales , Factores de Confusión Epidemiológicos , Heces/química , Femenino , Glucocorticoides/metabolismo , Masculino , Metaboloma , Modelos BiológicosRESUMEN
Snowshoe hares (Lepus americanus) maintain seasonal camouflage by molting to a white winter coat, but some hares remain brown during the winter in regions with low snow cover. We show that cis-regulatory variation controlling seasonal expression of the Agouti gene underlies this adaptive winter camouflage polymorphism. Genetic variation at Agouti clustered by winter coat color across multiple hare and jackrabbit species, revealing a history of recurrent interspecific gene flow. Brown winter coats in snowshoe hares likely originated from an introgressed black-tailed jackrabbit allele that has swept to high frequency in mild winter environments. These discoveries show that introgression of genetic variants that underlie key ecological traits can seed past and ongoing adaptation to rapidly changing environments.
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Mimetismo Biológico/fisiología , Liebres/fisiología , Pigmentación de la Piel/fisiología , Proteína de Señalización Agouti/genética , Animales , Mimetismo Biológico/genética , Regulación de la Expresión Génica , Variación Genética , Liebres/genética , Muda/genética , Muda/fisiología , Estaciones del Año , Pigmentación de la Piel/genéticaRESUMEN
Defining units that can be afforded legal protection is a crucial, albeit challenging, step in conservation planning. As we illustrate with a case study of the red wolf (Canis rufus) from the southeastern United States, this step is especially complex when the evolutionary history of the focal taxon is uncertain. The US Endangered Species Act (ESA) allows listing of species, subspecies, or Distinct Population Segments (DPSs) of vertebrates. Red wolves were listed as an endangered species in 1973, and their status remains precarious. However, some recent genetic studies suggest that red wolves are part of a small wolf species (C. lycaon) specialized for heavily forested habitats of eastern North America, whereas other authors suggest that red wolves arose, perhaps within the last ~400 years, through hybridization between gray wolves (C. lupus) and coyotes (C. latrans). Using published genetic, morphological, behavioral, and ecological data, we evaluated whether each evolutionary hypothesis would lead to a listable unit for red wolves. Although the potential hybrid origin of red wolves, combined with abundant evidence for recent hybridization with coyotes, raises questions about status as a separate species or subspecies, we conclude that under any proposed evolutionary scenario red wolves meet both criteria to be considered a DPS: they are Discrete compared with other conspecific populations, and they are Significant to the taxon to which they belong. As population-level units can qualify for legal protection under endangered-species legislation in many countries throughout the world, this general approach could potentially be applied more broadly.
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Especies en Peligro de Extinción , Lobos/genética , Animales , Conducta Animal , Ecosistema , Hibridación Genética , Estados Unidos , Lobos/fisiologíaRESUMEN
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.
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Aves/fisiología , Cambio Climático , Mamíferos/fisiología , Muda , Pigmentación , Animales , Estaciones del AñoRESUMEN
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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Biodiversidad , Mimetismo Biológico , Cambio Climático , Muda , Pigmentación , Animales , Estaciones del Año , VertebradosRESUMEN
Faecal glucocorticoid metabolite (FGM) concentrations are used increasingly as a non-invasive measure to index physiological stress experienced by diverse taxa. However, FGM may not be evenly distributed throughout a faecal mass or faecal pellet group. Moreover, within-sample variation in FGM measurements associated with different sampling and/or processing techniques is rarely reported despite potentially having important implications for inferring stress levels in free-ranging wildlife. Using a captive collection of snowshoe hares (Lepus americanus), we (i) assessed repeatability of FGM measurements (i.e. precision) from two processing techniques (measurements derived from dividing whole pellet groups into equal proportions prior to processing [G1], measurements from subsamples derived from thoroughly homogenized whole pellet groups [G2]) and (ii) conducted a power analysis to estimate sample-size requirements for detecting statistically significant differences in FGM concentrations at a population level. Our results indicate that the mean percent coefficient of variation (%CV) for within-sample FGM variation was slightly higher for G1 (%CV = 35, range 13.45-65.37) than for G2 (%CV = 23, range 7.26-47.94), though not statistically significant (two sample t-test, n = 8, t = 1.57, P = 0.16). Thus, FGM is relatively evenly distributed within snowshoe hare faecal pellet groups. However, subsampling from homogenized whole pellet groups may be more appropriate when the sampling time frame is less controlled (e.g. multiple defecation events) because a subsample derived from a homogenized whole pellet group might be more representative of the animal's 'average' physiological state compared to FGM concentrations derived from a few haphazardly selected faecal pellets. Power analysis results demonstrated the importance of a priori consideration of sample sizes. Relatively small effect sizes (e.g. <20%) may require sampling that is logistically and/or cost prohibitive. Yet for many situations of ecological or conservation interest, treatment effects may be substantial (>25%) and thus moderate sample sizes may be sufficient for testing research hypotheses regarding changes FGM concentrations.
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Understanding population dynamics requires reliable estimates of population density, yet this basic information is often surprisingly difficult to obtain. With rare or difficult-to-capture species, genetic surveys from noninvasive collection of hair or scat has proved cost-efficient for estimating densities. Here, we explored whether noninvasive genetic sampling (NGS) also offers promise for sampling a relatively common species, the snowshoe hare (Lepus americanus Erxleben, 1777), in comparison with traditional live trapping. We optimized a protocol for single-session NGS sampling of hares. We compared spatial capture-recapture population estimates from live trapping to estimates derived from NGS, and assessed NGS costs. NGS provided population estimates similar to those derived from live trapping, but a higher density of sampling plots was required for NGS. The optimal NGS protocol for our study entailed deploying 160 sampling plots for 4 days and genotyping one pellet per plot. NGS laboratory costs ranged from approximately $670 to $3000 USD per field site. While live trapping does not incur laboratory costs, its field costs can be considerably higher than for NGS, especially when study sites are difficult to access. We conclude that NGS can work for common species, but that it will require field and laboratory pilot testing to develop cost-effective sampling protocols.
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Seasonal coat colour change is an important adaptation to seasonally changing environments but the evolution of this and other circannual traits remains poorly understood. In this study, we use gene expression to understand seasonal coat colour moulting in wild snowshoe hares (Lepus americanus). We used hair colour to follow the progression of the moult, simultaneously sampling skin from three moulting stages in hares collected during the peak of the spring moult from white winter to brown summer pelage. Using RNA sequencing, we tested whether patterns of expression were consistent with predictions based on the established phases of the hair growth cycle. We found functionally consistent clustering across skin types, with 766 genes differentially expressed between moult stages. "White" pelage showed more differentially expressed genes that were upregulated relative to other skin types, involved in the transition between late telogen (quiescent stage) and the onset of anagen (proliferative stage). Skin samples from transitional "intermediate" and "brown" pelage were transcriptionally similar and resembled the regressive transition to catagen (regressive stage). We also detected differential expression of several key circadian clock and pigmentation genes, providing important means to dissect the bases of alternate seasonal colour morphs. Our results reveal that pelage colour is a useful biomarker for seasonal change but that there is a consistent lag between the main gene expression waves and change in visible coat colour. These experiments establish that developmental sampling from natural populations of nonmodel organisms can provide a crucial resource to dissect the genetic basis and evolution of complex seasonally changing traits.