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Proc Natl Acad Sci U S A. 2019 Nov 26;116(48):24150-24156. doi: 10.1073/pnas.1910471116. Epub 2019 Nov 11.

Introgression drives repeated evolution of winter coat color polymorphism in hares.

Author information

1
CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO), Rede de Investigação em Biodiversidade e Biologia Evolutiva (InBIO), Universidade do Porto, 4485-661 Vairão, Portugal.
2
Departamento de Biologia, Faculdade de Ciências, Universidade of Porto, 4169-007 Porto, Portugal.
3
Institut des Sciences de l'Évolution, Université de Montpellier, Centre National de la Recherche Scientifique, Institut de Recherche pour le Développement, École Pratique des Hautes Études, 34095 Montpellier, France.
4
Research Department, National Hunting and Wildlife Agency (ONCFS), 34990 Juvignac, France.
5
Department of Wildlife and Fishery Service Grison, CH-7001 Chur, Switzerland.
6
Institute of Wildlife Biology and Game Management, University of Natural Resources and Life Sciences, Vienna, 1180 Vienna, Austria.
7
Faculty of Science and Technology, University of the Faroe Islands, 100 Tórshavn, Faroe Islands.
8
CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO), Rede de Investigação em Biodiversidade e Biologia Evolutiva (InBIO), Universidade do Porto, 4485-661 Vairão, Portugal; jmeloferreira@cibio.up.pt.

Abstract

Changing from summer-brown to winter-white pelage or plumage is a crucial adaptation to seasonal snow in more than 20 mammal and bird species. Many of these species maintain nonwhite winter morphs, locally adapted to less snowy conditions, which may have evolved independently. Mountain hares (Lepus timidus) from Fennoscandia were introduced into the Faroe Islands in 1855. While they were initially winter-white, within ∼65 y all Faroese hares became winter-gray, a morph that occurs in the source population at low frequency. The documented population history makes this a valuable model for understanding the genetic basis and evolution of the seasonal trait polymorphism. Through whole-genome scans of differentiation and single-nucleotide polymorphism (SNP) genotyping, we associated winter coat color polymorphism to the genomic region of the pigmentation gene Agouti, previously linked to introgression-driven winter coat color variation in the snowshoe hare (Lepus americanus). Lower Agouti expression in the skin of winter-gray individuals during the autumn molt suggests that regulatory changes may underlie the color polymorphism. Variation in the associated genomic region shows signatures of a selective sweep in the Faroese population, suggesting that positive selection drove the fixation of the variant after the introduction. Whole-genome analyses of several hare species revealed that the winter-gray variant originated through introgression from a noncolor changing species, in keeping with the history of ancient hybridization between the species. Our findings show the recurrent role of introgression in generating winter coat color variation by repeatedly recruiting the regulatory region of Agouti to modulate seasonal coat color change.

KEYWORDS:

Lepus timidus; agouti signaling protein gene; genotype-phenotype; seasonal coat color change

PMID:
31712446
PMCID:
PMC6883779
[Available on 2020-05-11]
DOI:
10.1073/pnas.1910471116

Conflict of interest statement

The authors declare no competing interest.

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