skip to main content


Title: Museomics Dissects the Genetic Basis for Adaptive Seasonal Coloration in the Least Weasel
Abstract 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.  more » « less
Award ID(s):
1907022 1736249
NSF-PAR ID:
10341986
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Editor(s):
Teeling, Emma
Date Published:
Journal Name:
Molecular Biology and Evolution
Volume:
38
Issue:
10
ISSN:
1537-1719
Page Range / eLocation ID:
4388 to 4402
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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.

     
    more » « less
  2. null (Ed.)
    Abstract 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. 
    more » « less
  3. Abstract With novel human–wildlife interaction, predation regimes, and environmental conditions, in addition to often fragmented and smaller populations, urban areas present wildlife with altered natural selection parameters and genetic drift potential compared with nonurban regions. Plumage and pelage coloration in birds and mammals has evolved as a balance between avoiding detection by predator or prey, sexual selection, and thermoregulation. However, with altered mutation rates, reduced predation risk, increased temperatures, strong genetic drift, and increased interaction with people, the evolutionary contexts in which these colorations arose are radically different from what is present in urban areas. Regionally alternative color morphs or leucistic or melanistic individuals that aren't typical of most avian or mammalian populations may become more frequent as a result of adaptive or neutral evolution. Therefore, I conceptualize that, in urban areas, conspicuous color morphologies may persist, leading to an increase in the frequency of regionally atypical pelage coloration. In the present article, I discuss the potential for conspicuous color morphs to arise and persist in urban mammalian and avian populations, as well as the mechanisms for such persistence, as a result of altered environmental conditions and natural selection pressures. 
    more » « less
  4. Abstract Context

    Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.Fontaineais a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontaineaare subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.

    Objectives

    Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatenedFontaineaspecies. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis(Southern Fontainea) and critically endangeredF. oraria(Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.

    Methods

    We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.

    Results

    Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.

    Conclusions

    Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the twoFontaineaspecies. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.

     
    more » « less
  5. null (Ed.)
    Initially described in 1882, Chromis enchrysurus , the Yellowtail Reeffish, was redescribed in 1982 to account for an observed color morph that possesses a white tail instead of a yellow one, but morphological and geographic boundaries between the two color morphs were not well understood. Taking advantage of newly collected material from submersible studies of deep reefs and photographs from rebreather dives, this study sought to determine whether the white-tailed Chromis is actually a color morph of Chromis enchrysurus or a distinct species. Phylogenetic analyses of mitochondrial genes cytochrome b and cytochrome c oxidase subunit I separated Chromis enchrysurus and the white-tailed Chromis into two reciprocally monophyletic clades. A principal component analysis based on 27 morphological characters separated the two groups into clusters that correspond with caudal-fin coloration, which was either known or presumed based on the specimen’s collection site according to biogeographic data on species boundaries in the Greater Caribbean. Genetic, morphological, and biogeographic data all indicate that the white-tailed Chromis is a distinct species, herein described as Chromis vanbebberae sp. nov. The discovery of a new species within a conspicuous group such as damselfishes in a well-studied region of the world highlights the importance of deep-reef exploration in documenting undiscovered biodiversity. 
    more » « less