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Mol Biol Evol. 2021 Sep 27;38(10):4388-4402. doi: 10.1093/molbev/msab177.

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

Molecular biology and evolution

Inês Miranda, Iwona Giska, Liliana Farelo, João Pimenta, Marketa Zimova, Jarosław Bryk, Love Dalén, L Scott Mills, Karol Zub, José Melo-Ferreira

Affiliations

  1. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal.
  2. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, 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.
  6. Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden.
  7. Wildlife Biology Program, University of Montana, Missoula, MT, USA.
  8. Office of Research and Creative Scholarship, University of Montana, Missoula, MT, USA.
  9. Mammal Research Institute, Polish Academy of Sciences, Bia?owie?a, Poland.

PMID: 34157721 PMCID: PMC8476133 DOI: 10.1093/molbev/msab177

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.

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Keywords: Mustela nivalis ; genotype–phenotype association; melanocortin-1 receptor gene; natural history collections; seasonal coat color change

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