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Introgression Drives Repeated Evolution of Winter Coat Color Polymorphism in Hares

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Introgression Drives Repeated Evolution of Winter Coat Color Polymorphism in Hares Introgression drives repeated evolution of winter coat color polymorphism in hares Iwona Giskaa, Liliana Fareloa, João Pimentaa, Fernando A. Seixasa,b,c, Mafalda S. Ferreiraa,b, João P. Marquesa,b,c, Inês Mirandaa,b, Jérôme Lettyd, Hannes Jennye, Klaus Hackländerf, Eyðfinn Magnusseng, and José Melo-Ferreiraa,b,1 aCIBIO-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; bDepartamento de Biologia, Faculdade de Ciências, Universidade of Porto, 4169-007 Porto, Portugal; cInstitut 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; dResearch Department, National Hunting and Wildlife Agency (ONCFS), 34990 Juvignac, France; eDepartment of Wildlife and Fishery Service Grison, CH-7001 Chur, Switzerland; fInstitute of Wildlife Biology and Game Management, University of Natural Resources and Life Sciences, Vienna, 1180 Vienna, Austria; and gFaculty of Science and Technology, University of the Faroe Islands, 100 Tórshavn, Faroe Islands Edited by Leif Andersson, Uppsala University, Uppsala, Sweden, and approved October 15, 2019 (received for review June 19, 2019) Changing from summer-brown to winter-white pelage or plumage is caused by climate change, which endangers winter-white populations a crucial adaptation to seasonal snow in more than 20 mammal and (7, 10). Understanding the emergence of seasonal coat color bird species. Many of these species maintain nonwhite winter polymorphisms is therefore crucial for quantifying the adaptive morphs, locally adapted to less snowy conditions, which may potential of seasonal coat color changing species facing climate have evolved independently. Mountain hares (Lepus timidus) from change (10, 11). Fennoscandia were introduced into the Faroe Islands in 1855. Of the >30 species of hares (Lepus spp.), 6 undergo seasonal While they were initially winter-white, within ∼65 y all Faroese coat color molts, often maintaining within-species variation in hares became winter-gray, a morph that occurs in the source pop- winter pelage color (10). In snowshoe hares (Lepus americanus), ulation at low frequency. The documented population history makes winter-white/winter-brown polymorphism maps to the agouti sig- this a valuable model for understanding the genetic basis and evo- naling protein gene (ASIP; Agouti) and is driven by cis-regulatory lution of the seasonal trait polymorphism. Through whole-genome changes influencing the expression of the gene (11). The winter- EVOLUTION scans of differentiation and single-nucleotide polymorphism (SNP) brown variant introgressed from the neighboring black-tailed genotyping, we associated winter coat color polymorphism to the jackrabbit (Lepus californicus), a winter-brown species, seeding genomic region of the pigmentation gene Agouti, previously linked adaptation to the warmer coastal habitat with less winter snow in to introgression-driven winter coat color variation in the snowshoe the Pacific Northwest region in North America. Winter variation hare (Lepus americanus). Lower Agouti expression in the skin of in coat color has also been studied in arctic foxes (Vulpes lagopus), winter-gray individuals during the autumn molt suggests that reg- where melanocortin 1 receptor gene (MC1R) mutations induce the ulatory changes may underlie the color polymorphism. Variation in expression of a blue-gray winter phenotype instead of the pre- the associated genomic region shows signatures of a selective dominant winter-white (12). These results implicate the MC1R-Agouti sweep in the Faroese population, suggesting that positive selec- tion drove the fixation of the variant after the introduction. Whole- Significance genome analyses of several hare species revealed that the winter-gray variant originated through introgression from a noncolor changing Seasonal molts to winter-white pelage or plumage are key ad- species, in keeping with the history of ancient hybridization between aptations to seasonal snow in over 20 animal species. However, the species. Our findings show the recurrent role of introgression in winter color polymorphism within species is crucial for adapta- generating winter coat color variation by repeatedly recruiting the tion to environmental heterogeneity and provides striking regulatory region of Agouti to modulate seasonal coat color change. models to tackle the basis of repeated evolution. We show that the pigmentation gene Agouti, which underlies introgression- seasonal coat color change | agouti signaling protein gene | Lepus driven winter color variation in snowshoe hares, is also associated timidus | genotype-phenotype with winter-white/winter-grey polymorphism in mountain hares, possibly due to altered expression of the gene. The winter-grey ecurrent evolution has puzzled evolutionary biologists for variant introgressed into the mountain hare through hybridiza- Rdecades (1, 2). While controlled experiments testing the re- tion with a noncolor changing species. These findings show that peated nature of evolution are possible in only a few models, the same genomic region was repeatedly recruited to determine comparative evolutionary studies of similar traits that may have winter coat color in different hare species, highlighting the re- evolved independently in closely related taxa provide powerful current role of introgression in generating phenotypic variation. means to understand recurrent evolution at different levels, from processes to phenotypes and their molecular basis (3–5). Seasonal Author contributions: I.G., E.M., and J.M.-F. designed research; I.G., L.F., M.S.F., J.L., H.J., pelage or plumage color change is a key adaptive phenological trait K.H., E.M., and J.M.-F. performed research; I.G., J.P., F.A.S., M.S.F., J.P.M., I.M., and J.M.-F. of over 20 vertebrates, such as hares, weasels, and grouse, which analyzed data; I.G. and J.M.-F. wrote the paper; and J.M.-F. coordinated the study. inhabit environments with seasonal snow cover (6). Photoperiod- The authors declare no competing interest. controlled pelage molts from summer-browntowinter-whitecoats This article is a PNAS Direct Submission. allow the maintenance of camouflage year-round, reducing the Published under the PNAS license. fitness costs of increased predation due to coat-background color Data deposition: All original high-throughput sequencing data reported in this article mismatch (7–9). However, genetically determined winter coat color have been deposited in the Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) under BioProjects PRJNA564335 (IDs SAMN12710256 to SAMN12710314)and polymorphism exists in many of these species, maintained by clinal PRJNA562432 (ID SAMN12640762). Genotyping data generated in this work are provided selective pressures correlated with snow cover environmental var- in SI Appendix, Tables S6 and S7. iables (10). The occurrence of winter coat color variation across 1To whom correspondence may be addressed. Email: [email protected]. species provides valuable models to dissect pathways for recurrent This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. phenotypic evolution. Also, such polymorphism may provide stand- 1073/pnas.1910471116/-/DCSupplemental. ing variation to enable rapid adaptation to snow cover reductions www.pnas.org/cgi/doi/10.1073/pnas.1910471116 PNAS Latest Articles | 1of7 Downloaded by guest on October 2, 2021 melanin pigmentation system, often involved in permanent pelage individual coverage from individually barcoded libraries. Three color variation in mammals (13), in the evolution of seasonal populations were sampled: hares from the Faroe Islands (winter- changes in coloration. However, little is known about the evolu- gray; n = 20 individuals; 16.8× population depth), Fennoscandia tion of seasonal coat color variation across species. (the source population of the Faroese hares; winter-white; n = Here, we study the genetic basis and evolution of winter coat 19; 18.0×), and the Alps (winter-white; n = 20; 17.1×) (Fig. 1C color polymorphism, using the winter-white/winter-gray coat and SI Appendix, Tables S1 and S2). One Faroese hare was se- color variation in mountain hares (Lepus timidus). In most of the quenced at higher depth (6.9×; SI Appendix, Table S3). Reads species’ range, mountain hares molt to winter-white coats, but were mapped to a hare pseudoreference genome (97% mapped alternative winter color morphs occur in the species. For exam- reads on average per specimen; SI Appendix, Table S2), built ple, in Ireland mountain hares remain brown year-round, and in through iterative mapping to the European rabbit (Oryctolagus Fennoscandia a winter-gray morph exists (i.e., the heath-hare; cuniculus) genome (from ref. 19; ref. 20). Principal component also called blue-gray) in addition to the predominant winter- analysis of genetic variation (123,995 single-nucleotide polymor- white morph (Fig. 1 A and B) (14, 15). Winter-gray mountain phisms, SNPs) showed 3 groups, corresponding to the geographic hares were common in southern Sweden but have become pro- origin of specimens (SI Appendix,Fig.S1A). Phylogenies based on gressively rarer since the early 20th century, likely due to a population allele counts (136,834 sites) (Fig. 1D) and on individual combination of predation by the red fox (Vulpes
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