Introgression drives repeated evolution of winter coat color polymorphism in hares

Iwona Giska, Liliana Farelo, João Pimenta, Fernando A. Seixas, Mafalda S. Ferreira, João P. Marques, Inês Miranda, Jérôme Letty, Hannes Jenny, Klaus Hackländer, Eyðfinn Magnussen, José Melo-Ferreira

Research output: Contribution to journalArticlepeer-review

22 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)24150-24156
Number of pages7
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number48
DOIs
Publication statusPublished - 26 Nov 2019

Keywords

  • Agouti signaling protein gene
  • Genotype-phenotype
  • Lepus timidus
  • Seasonal coat color change

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