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

Journal Article · · Molecular Biology and Evolution (Online)
 [1];  [2];  [2];  [2];  [3];  [4];  [5];  [6];  [7]; ORCiD logo [1];
  1. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal, Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, Portugal
  2. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal
  3. School for Environment and Sustainability, University of Michigan, Ann Arbor, MI, USA
  4. School of Applied Sciences, University of Huddersfield, Quennsgate, Huddersfield, United Kingdom
  5. Centre for Palaeogenetics, Stockholm, Sweden, Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden
  6. Wildlife Biology Program, University of Montana, Missoula, MT, USA, Office of Research and Creative Scholarship, University of Montana, Missoula, MT, USA
  7. Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland

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.

Sponsoring Organization:
USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain
OSTI ID:
1822505
Journal Information:
Molecular Biology and Evolution (Online), Journal Name: Molecular Biology and Evolution (Online) Journal Issue: 10 Vol. 38; ISSN 1537-1719
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (86)

Amino Acid Properties and Consequences of Substitutions book December 2002
Transcriptomic regulation of seasonal coat color change in hares journal January 2020
The role of melanocyte-stimulating hormone (MSH) receptor in bovine coat color determination journal September 1995
Melanocortin 1 receptor variation in the domestic dog journal January 2000
Molecular and pharmacological characterization of dominant black coat color in sheep journal January 1999
Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function journal March 1993
How many principal components? stopping rules for determining the number of non-trivial axes revisited journal June 2005
Museum Genomics Confirms that the Lord Howe Island Stick Insect Survived Extinction journal October 2017
Historical Genomes Reveal the Genomic Consequences of Recent Population Decline in Eastern Gorillas journal January 2019
The use of museum specimens with high-throughput DNA sequencers journal February 2015
Two cysteine substitutions in the MC1R generate the blue variant of the arctic fox (Alopex lagopus) and prevent expression of the white winter coat journal October 2005
A coalescent model for the effect of advantageous mutations on the genealogy of a population journal October 2005
Vertebrate pigmentation: from underlying genes to adaptive function journal May 2010
Next-generation museum genomics: Phylogenetic relationships among palpimanoid spiders using sequence capture techniques (Araneae: Palpimanoidea) journal October 2018
Agouti protein is an antagonist of the melanocyte-stimulating-hormone receptor journal October 1994
Phylogeography of the weasel (Mustela nivalis) in the western-Palaearctic region: combined effects of glacial events and human movements journal January 2010
The draft genome sequence of the ferret (Mustela putorius furo) facilitates study of human respiratory disease journal November 2014
A non-epistatic interaction of agouti and extension in the fox, Vulpes vulpes journal March 1997
jModelTest 2: more models, new heuristics and parallel computing journal July 2012
Ecological genomics of local adaptation journal October 2013
Rab27a co-ordinates actin-dependent transport by controlling organelle-associated motors and track assembly proteins journal July 2020
Climate change is affecting mortality of weasels due to camouflage mismatch journal May 2018
Decline of the boreal willow grouse (Lagopus lagopus) has been accelerated by more frequent snow-free springs journal April 2020
Patterns of damage in genomic DNA sequences from a Neandertal journal August 2007
Microarray analysis sheds light on the dedifferentiating role of agouti signal protein in murine melanocytes via the Mc1r journal January 2009
Camouflage mismatch in seasonal coat color due to decreased snow duration journal April 2013
Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments journal September 2013
Introgression drives repeated evolution of winter coat color polymorphism in hares journal November 2019
Bayes Factors journal June 1995
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses journal September 2007
The Origin and Spread of Locally Adaptive Seasonal Camouflage in Snowshoe Hares journal September 2020
SNPassoc: an R package to perform whole genome association studies journal January 2007
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
The Sequence Alignment/Map format and SAMtools journal June 2009
MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus journal June 2010
PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq) journal October 2011
PEAR: a fast and accurate Illumina Paired-End reAd mergeR journal October 2013
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Efficient Bayesian inference under the structured coalescent journal April 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data journal October 2015
Versatile genome assembly evaluation with QUAST-LG journal June 2018
Melanocortin Receptor 1 (MC1R) Mutations and Coat Color in Pigs journal November 1998
The Effect of Ancient DNA Damage on Inferences of Demographic Histories journal July 2008
Detecting Selective Sweeps from Pooled Next-Generation Sequencing Samples journal March 2012
SweeD: Likelihood-Based Detection of Selective Sweeps in Thousands of Genomes journal June 2013
FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program: Table 1. journal June 2015
Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform journal October 2011
SIFT web server: predicting effects of amino acid substitutions on proteins journal June 2012
Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7 journal April 2018
Biological collections for understanding biodiversity in the Anthropocene
  • Meineke, Emily K.; Davies, T. Jonathan; Daru, Barnabas H.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1763 https://doi.org/10.1098/rstb.2017.0386
journal November 2018
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data journal July 2010
Comparative Recombination Rates in the Rat, Mouse, and Human Genomes journal April 2004
Direct determination of diploid genome sequences journal April 2017
Illumina Sequencing Library Preparation for Highly Multiplexed Target Capture and Sequencing journal June 2010
Pool‐hmm: a Python program for estimating the allele frequency spectrum and detecting selective sweeps from next generation sequencing of pooled samples journal January 2013
Improving the estimation of genetic distances from Next-Generation Sequencing data: Genetic Distances from NGS Data journal March 2015
Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world? journal March 2018
An experimental translocation identifies habitat features that buffer camouflage mismatch in snowshoe hares journal November 2018
High fitness costs of climate change‐induced camouflage mismatch journal January 2016
Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range* journal May 2020
Pharmacological Characterization of Loss of Function Mutations of the Human Melanocortin 1 Receptor That Are Associated with Red Hair journal November 2004
Climate and refugial origin influence the mitochondrial lineage distribution of weasels (Mustela nivalis) in a phylogeographic suture zone: CLIMATE INFLUENCES mtDNA DISTRIBUTION journal February 2012
Melanocortin‐1 receptor structure and functional regulation journal November 2005
Population genomics based on low coverage sequencing: how low should we go? journal November 2012
Unlocking the vault: next-generation museum population genomics journal October 2013
Natural history collections as windows on evolutionary processes journal February 2016
The transcriptional landscape of seasonal coat colour moult in the snowshoe hare journal June 2017
The Developmental Role of Agouti in Color Pattern Evolution journal February 2011
Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change journal February 2018
Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares journal June 2018
The Response of Northern Hemisphere Snow Cover to a Changing Climate journal April 2009
Decomposing the Apoptosis Pathway Into Biologically Interpretable Principal Components journal January 2018
BLAST+: architecture and applications journal January 2009
BEAST: Bayesian evolutionary analysis by sampling trees journal January 2007
Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation journal February 2008
A Ligand-Mimetic Model for Constitutive Activation of the Melanocortin-1 Receptor journal April 1998
Expression and transgenic studies of the mouse agouti gene provide insight into the mechanisms by which mammalian coat color patterns are generated journal October 1995
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis journal April 2014
Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data journal November 2012
Robust Demographic Inference from Genomic and SNP Data journal October 2013
Temporal genomic contrasts reveal rapid evolutionary responses in an alpine mammal during recent climate change journal May 2019
PoPoolation: A Toolbox for Population Genetic Analysis of Next Generation Sequencing Data from Pooled Individuals journal January 2011
Climate Change and Human Disturbance Can Lead to Local Extinction of Alpine Rock Ptarmigan: New Insight from the Western Italian Alps journal November 2013
Estimating Individual Admixture Proportions from Next Generation Sequencing Data journal September 2013
Identifying and Classifying Shared Selective Sweeps from Multilocus Data journal May 2020