Genomic signatures of climate adaptation in bank voles

. 2024 Mar ; 14 (3) : e10886. [epub] 20240307

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38455148

Evidence for divergent selection and adaptive variation across the landscape can provide insight into a species' ability to adapt to different environments. However, despite recent advances in genomics, it remains difficult to detect the footprints of climate-mediated selection in natural populations. Here, we analysed ddRAD sequencing data (21,892 SNPs) in conjunction with geographic climate variation to search for signatures of adaptive differentiation in twelve populations of the bank vole (Clethrionomys glareolus) distributed across Europe. To identify the loci subject to selection associated with climate variation, we applied multiple genotype-environment association methods, two univariate and one multivariate, and controlled for the effect of population structure. In total, we identified 213 candidate loci for adaptation, 74 of which were located within genes. In particular, we identified signatures of selection in candidate genes with functions related to lipid metabolism and the immune system. Using the results of redundancy analysis, we demonstrated that population history and climate have joint effects on the genetic variation in the pan-European metapopulation. Furthermore, by examining only candidate loci, we found that annual mean temperature is an important factor shaping adaptive genetic variation in the bank vole. By combining landscape genomic approaches, our study sheds light on genome-wide adaptive differentiation and the spatial distribution of variants underlying adaptive variation influenced by local climate in bank voles.

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Aars, J. , Ims, R. A. , Liu, H. P. , Mulvey, M. , & Smith, M. H. (1998). Bank voles in linear habitats show restricted gene flow as revealed by mitochondrial DNA (mtDNA). Molecular Ecology, 7(10), 1383–1389. PubMed

Abramson, N. I. , Rodchenkova, E. N. , & Kostygov, A. Y. (2009). Genetic variation and phylogeography of the bank vole (Clethrionomys glareolus, Arvicolinae, Rodentia) in Russia with special reference to the introgression of the mtDNA of a closely related species, red‐backed vole (Cl. Rutilus). Russian Journal of Genetics, 45(5), 533–545. 10.1134/S1022795409050044 PubMed DOI

Alexa, J. , & Rahnenführer, J. (2010). TopGO: Enrichment analysis for gene ontology, R package version 2(0) (Bioconductor) . R package version 2.22.0.

Andrew, S. C. , Jensen, H. , Hagen, I. J. , Lundregan, S. , & Griffith, S. C. (2018). Signatures of genetic adaptation to extremely varied Australian environments in introduced European house sparrows. Molecular Ecology, 27(22), 4542–4555. 10.1111/mec.14897 PubMed DOI

Arthur, J. S. C. , & Ley, S. C. (2013). Mitogen‐activated protein kinases in innate immunity. Nature Reviews Immunology, 13(9), 679–692. 10.1038/nri3495 PubMed DOI

Babin, C. , Gagnaire, P. A. , Pavey, S. A. , & Bernatchez, L. (2017). RAD‐Seq reveals patterns of additive polygenic variation caused by spatially‐varying selection in the American eel Anguilla rostrata . Genome Biology and Evolution, 9(11), 2974–2986. 10.1093/gbe/evx226 PubMed DOI PMC

Baker, J. , Liu, J. P. , Robertson, E. J. , & Efstratiadis, A. (1993). Role of insulin‐like growth factors in embryonic and postnatal growth. Cell, 75(1), 73–82. 10.1016/S0092-8674(05)80085-6 PubMed DOI

Ballinger, M. A. , & Nachman, M. W. (2022). The contribution of genetic and environmental effects to Bergmann's rule and Allen's rule in house mice. The American Naturalist, 199(5), 691–704. 10.1086/719028 PubMed DOI

Balzani, E. , Lassi, G. , Maggi, S. , Sethi, S. , Parsons, M. J. , Simon, M. , Nolan, P. M. , & Tucci, V. (2016). The Zfhx3‐mediated axis regulates sleep and interval timing in mice. Cell Reports, 16(3), 615–621. 10.1016/j.celrep.2016.06.017 PubMed DOI PMC

Barañano, D. E. , Rao, M. , Ferris, C. D. , & Snyder, S. H. (2002). Biliverdin reductase: A major physiologic cytoprotectant. Proceedings of the National Academy of Sciences of the United States of America, 99(25), 16093–16098. 10.1073/pnas.252626999 PubMed DOI PMC

Barghi, N. , Hermisson, J. , & Schlötterer, C. (2020). Polygenic adaptation: A unifying framework to understand positive selection. Nature Reviews Genetics, 21(12), 769–781. 10.1038/s41576-020-0250-z PubMed DOI

Beckman, E. J. , Martins, F. , Suzuki, T. A. , Bi, K. , Keeble, S. , Good, J. M. , Chavez, A. S. , Ballinger, M. A. , Agwamba, K. , & Nachman, M. W. (2022). The genomic basis of high‐elevation adaptation in wild house mice (Mus musculus domesticus) from South America. Genetics, 220(2), iyab226. 10.1093/genetics/iyab226 PubMed DOI PMC

Benjamini, Y. , & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B Methodological, 57(1), 289–300.

Berryman, D. E. , Glad, C. A. M. , List, E. O. , & Johannsson, G. (2013). The GH/IGF‐1 axis in obesity: Pathophysiology and therapeutic considerations. Nature Reviews Endocrinology, 9(6), 346–356. 10.1038/nrendo.2013.64 PubMed DOI

Birsoy, K. , Festuccia, W. T. , & Laplante, M. (2013). A comparative perspective on lipid storage in animals. Journal of Cell Science, 126(7), 1541–1552. 10.1242/jcs.104992 PubMed DOI

Bradburd, G. S. , Ralph, P. L. , & Coop, G. M. (2013). Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution; International Journal of Organic Evolution, 67(11), 3258–3273. 10.1111/evo.12193 PubMed DOI PMC

Cannon, B. , & Nedergaard, J. (2004). Brown adipose tissue: Function and physiological significance. Physiological Reviews, 84(1), 277–359. 10.1152/physrev.00015.2003 PubMed DOI

Capblancq, T. , Luu, K. , Blum, M. G. B. B. , Bazin, E. , & Bazin, É. (2018). Evaluation of redundancy analysis to identify signatures of local adaptation. Molecular Ecology Resources, 18(6), 1223–1233. 10.1111/1755-0998.12906 PubMed DOI

Cattell, R. B. (1966). The scree test for the number of factors. Multivariate Behavioral Research, 1(2), 245–276. 10.1207/s15327906mbr0102_10 PubMed DOI

Colosimo, P. F. , Hosemann, K. E. , Balabhadra, S. , Villarreal, G. , Dickson, H. , Grimwood, J. , Schmutz, J. , Myers, R. M. , Schluter, D. , & Kingsley, D. M. (2005). Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307(5717), 1928–1933. 10.1126/science.1107239 PubMed DOI

Coop, G. , Witonsky, D. B. , Di Rienzo, A. , & Pritchard, J. K. (2010). Using environmental correlations to identify loci underlying local adaptation. Genetics, 185(4), 1411–1423. 10.1534/genetics.110.114819 PubMed DOI PMC

Cresko, W. A. , Amores, A. , Wilson, C. , Murphy, J. , Currey, M. , Phillips, P. , Bell, M. A. , Kimmel, C. B. , & Postlethwait, J. H. (2004). Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proceedings of the National Academy of Sciences of the United States of America, 101(16), 6050–6055. 10.1073/pnas.0308479101 PubMed DOI PMC

de Villemereuil, P. , Frichot, E. , Bazin, É. , François, O. , & Gaggiotti, O. E. (2014). Genome scan methods against more complex models: When and how much should we trust them? Molecular Ecology, 23(8), 2006–2019. 10.1111/mec.12705 PubMed DOI

Deffontaine, V. , Libois, R. , Kotlík, P. , Sommer, R. , Nieberding, C. , Paradis, E. , Searle, J. B. , & Michaux, J. R. (2005). Beyond the Mediterranean peninsulas: Evidence of central European glacial refugia for a temperate forest mammal species, the bank vole Clethrionomys glareolus . Molecular Ecology, 14(6), 1727–1739. 10.1111/j.1365-294X.2005.02506.x PubMed DOI

Deter, J. , Bryja, J. , Chaval, Y. , Galan, M. , Henttonen, H. , Laakkonen, J. , Voutilainen, L. , Vapalahti, O. , Vaheri, A. , Salvador, A. R. , Morand, S. , Cosson, J. F. , & Charbonnel, N. (2008). Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole. Infection, Genetics and Evolution, 8(4), 450–458. 10.1016/j.meegid.2007.07.003 PubMed DOI

Dixon, P. (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14(6), 927–930. 10.1111/j.1654-1103.2003.tb02228.x DOI

Dubois, A. , Galan, M. , Cosson, J. F. , Gauffre, B. , Henttonen, H. , Niemimaa, J. , Razzauti, M. , Voutilainen, L. , Vitalis, R. , Guivier, E. , & Charbonnel, N. (2017). Microevolution of bank voles (Myodes glareolus) at neutral and immune‐related genes during multiannual dynamic cycles: Consequences for Puumala hantavirus epidemiology. Infection, Genetics and Evolution, 49, 318–329. 10.1016/j.meegid.2016.12.007 PubMed DOI

Eaton, D. A. R. (2014). PyRAD: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics, 30(13), 1844–1849. 10.1093/bioinformatics/btu121 PubMed DOI

Fan, S. , Hansen, M. E. B. , Lo, Y. , & Tishkoff, S. A. (2016). Going global by adapting local: A review of recent human adaptation. Science, 354(6308), 54–59. 10.1126/science.aaf5098 PubMed DOI PMC

Fick, S. E. , & Hijmans, R. J. (2017). WorldClim 2: New 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. 10.1002/joc.5086 DOI

Filipi, K. , Marková, S. , Searle, J. B. , & Kotlík, P. (2015). Mitogenomic phylogenetics of the bank vole Clethrionomys glareolus, a model system for studying end‐glacial colonization of Europe. Molecular Phylogenetics and Evolution, 82, 245–257. 10.1016/j.ympev.2014.10.016 PubMed DOI

Forester, B. R. , Lasky, J. R. , Wagner, H. H. , & Urban, D. L. (2018). Comparing methods for detecting multilocus adaptation with multivariate genotype–environment associations. Molecular Ecology, 27(9), 2215–2233. 10.1111/mec.14584 PubMed DOI

Frichot, E. , & François, O. (2015). LEA: An R package for landscape and ecological association studies. Methods in Ecology and Evolution, 6(8), 925–929. 10.1111/2041-210x.12382 DOI

Frichot, E. , Schoville, S. D. , Bouchard, G. , & François, O. (2013). Testing for associations between loci and environmental gradients using latent factor mixed models. Molecular Biology and Evolution, 30(7), 1687–1699. 10.1093/molbev/mst063 PubMed DOI PMC

Frichot, E. , Schoville, S. D. , de Villemereuil, P. , Gaggiotti, O. E. , & Francois, O. (2015). Detecting adaptive evolution based on association with ecological gradients: Orientation matters! Heredity, 115(1), 22–28. 10.1038/hdy.2015.7 PubMed DOI PMC

Fumagalli, M. , Moltke, I. , Grarup, N. , Racimo, F. , Bjerregaard, P. , Jørgensen, M. E. , Korneliussen, T. S. , Gerbault, P. , Skotte, L. , Linneberg, A. , Christensen, C. , Brandslund, I. , Jørgensen, T. , Huerta‐Sánchez, E. , Schmidt, E. B. , Pedersen, O. , Hansen, T. , Albrechtsen, A. , & Nielsen, R. (2015). Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science, 349(6254), 1343–1347. 10.1126/science.aab2319 PubMed DOI

Fumagalli, M. , Vieira, F. G. , Linderoth, T. , & Nielsen, R. (2014). NgsTools: Methods for population genetics analyses from next‐generation sequencing data. Bioinformatics, 30(10), 1486–1487. 10.1093/bioinformatics/btu041 PubMed DOI PMC

Gagnaire, P.‐A. , & Gaggiotti, O. E. (2016). Detecting polygenic selection in marine populations by combining population genomics and quantitative genetics approaches. Current Zoology, 62(6), 603–616. 10.1093/cz/zow088 PubMed DOI PMC

Gansauge, M. T. , & Meyer, M. (2013). Single‐stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nature Protocols, 8(4), 737–748. 10.1038/nprot.2013.038 PubMed DOI

Gerlach, G. , & Musolf, K. (2000). Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology, 14(4), 1066–1074. 10.1046/j.1523-1739.2000.98519.x DOI

Gil‐Iturbe, E. , Arbones‐Mainar, J. M. , Moreno‐Aliaga, M. J. , & Lostao, M. P. (2019). GLUT12 and adipose tissue: Expression, regulation and its relation with obesity in mice. Acta Physiologica, 226(4), e13283. 10.1111/apha.13283 PubMed DOI

Grau, J. H. , Hackl, T. , Koepfli, K. P. , & Hofreiter, M. (2018). Improving draft genome contiguity with reference‐derived in silico mate‐pair libraries. GigaScience, 7(5), giy029. 10.1093/gigascience/giy029 PubMed DOI PMC

Gray, J. , Yeo, G. , Hung, C. , Keogh, J. , Clayton, P. , Banerjee, K. , McAulay, A. , O'Rahilly, S. , & Farooqi, I. S. (2007). Functional characterization of human NTRK2 mutations identified in patients with severe early‐onset obesity. International Journal of Obesity, 31(2), 359–364. 10.1038/sj.ijo.0803390 PubMed DOI

Grundy, G. J. , Rulten, S. L. , Zeng, Z. , Arribas‐Bosacoma, R. , Iles, N. , Manley, K. , Oliver, A. , & Caldecott, K. W. (2012). APLF promotes the assembly and activity of non‐homologous end joining protein complexes. The EMBO Journal, 32(1), 112–125. 10.1038/emboj.2012.304 PubMed DOI PMC

Grosiak, M. , Koteja, P. , Bauchinger, U. , & Sadowska, E. T. (2020). Age‐related changes in the thermoregulatory properties in bank voles from a selection experiment. Frontiers in Physiology, 11, 1408. 10.3389/fphys.2020.576304 PubMed DOI PMC

Guivier, E. , Galan, M. , Chaval, Y. , Xuéreb, A. , Ribas Salvador, A. , Poulle, M. , Voutilainen, L. , Henttonen, H. , Charbonnel, N. , & Cosson, J. F. (2011). Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus. Molecular Ecology, 20(17), 3569–3583. PubMed

Guivier, E. , Galan, M. , Henttonen, H. , Cosson, J. F. , & Charbonnel, N. (2014). Landscape features and helminth co‐infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology. Heredity, 112(3), 274–281. 10.1038/hdy.2013.103 PubMed DOI PMC

Günther, T. , & Coop, G. (2013). Robust identification of local adaptation from allele frequencies. Genetics, 195(1), 205–220. 10.1534/genetics.113.152462 PubMed DOI PMC

Haasl, R. J. , & Payseur, B. A. (2016). Fifteen years of genomewide scans for selection: Trends, lessons and unaddressed genetic sources of complication. Molecular Ecology, 25(1), 5–23. 10.1111/mec.13339 PubMed DOI PMC

Hancock, A. M. , Brachi, B. , Faure, N. , Horton, M. W. , Jarymowycz, L. B. , Sperone, F. G. , Toomajian, C. , Roux, F. , & Bergelson, J. (2011). Adaptation to climate across the Arabidopsis thaliana genome. Science, 334(6052), 83–86. 10.1126/science.1209244 PubMed DOI

Harris, R. S. (2007). Improved pairwise alignment of genomic DNA . Ph.D [PhD Thesis]. In The Pennsylvania State University. United States—Pennsylvania.

Harris, S. E. , & Munshi‐South, J. (2017). Signatures of positive selection and local adaptation to urbanization in white‐footed mice Peromyscus leucopus . Molecular Ecology, 26(22), 6336–6350. 10.1111/mec.14369 PubMed DOI PMC

Harrison, P. M. , Gutowsky, L. F. G. , Martins, E. G. , Ward, T. D. , Patterson, D. A. , Cooke, S. J. , & Power, M. (2017). Individual isotopic specializations predict subsequent inter‐individual variation in movement in a freshwater fish. Ecology, 98(3), 608–615. 10.1002/ecy.1681 PubMed DOI

Hayashi, T. , Nozaki, Y. , Nishizuka, M. , Ikawa, M. , Osada, S. , & Imagawa, M. (2011). Factor for adipocyte differentiation 158 gene disruption prevents the body weight gain and insulin resistance induced by a high‐fat diet. Biological and Pharmaceutical Bulletin, 34(8), 1257–1263. 10.1248/bpb.34.1257 PubMed DOI

Horniková, M. , Marková, S. , Lanier, H. C. , Searle, J. B. , & Kotlik, P. (2021). A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole. Ecology and Evolution, 11(12), 8215–8225. PubMed PMC

Houtz, J. , Liao, G.‐Y. , An, J. J. , & Xu, B. (2021). Discrete TrkB‐expressing neurons of the dorsomedial hypothalamus regulate feeding and thermogenesis. Proceedings of the National Academy of Sciences, 118(4), e2017218118. 10.1073/pnas.2017218118 PubMed DOI PMC

Iles, K. E. , & Forman, H. J. (2002). Macrophage signaling and respiratory burst. Immunologic Research, 26(1), 95–105. 10.1385/IR:26:1-3:095 PubMed DOI

Joost, S. , Bonin, A. , Bruford, M. W. , Després, L. , Conord, C. , Erhardt, G. , & Taberlet, P. (2007). A spatial analysis method (SAM) to detect candidate loci for selection: Towards a landscape genomics approach to adaptation. Molecular Ecology, 16(18), 3955–3969. PubMed

Kanematsu, T. , Oue, K. , Okumura, T. , Harada, K. , Yamawaki, Y. , Asano, S. , Mizokami, A. , Irifune, M. , & Hirata, M. (2019). Phospholipase C‐related catalytically inactive protein: A novel signaling molecule for modulating fat metabolism and energy expenditure. Journal of Oral Biosciences, 61(2), 65–72. 10.1016/j.job.2019.04.002 PubMed DOI

Kaplan, M. H. (2005). STAT4: A critical regulator of inflammation in vivo . Immunologic Research, 31(3), 231–241. 10.1385/IR:31:3:231 PubMed DOI

Kawecki, T. J. , & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7(12), 1225–1241. 10.1111/j.1461-0248.2004.00684.x DOI

Klaus, S. , Heldmaier, G. , & Ricquier, D. (1988). Seasonal acclimation of bank voles and wood mice: Nonshivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. Journal of Comparative Physiology B, 158(2), 157–164. 10.1007/BF01075829 PubMed DOI

Korneliussen, T. S. , Moltke, I. , Albrechtsen, A. , & Nielsen, R. (2013). Calculation of Tajima's D and other neutrality test statistics from low depth next‐generation sequencing data. BMC Bioinformatics, 14(1), 289. 10.1186/1471-2105-14-289 PubMed DOI PMC

Kotlik, P. , Deffontaine, V. , Mascheretti, S. , Zima, J. , Michaux, J. R. , & Searle, J. B. (2006). A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences of the United States of America, 103(40), 14860–14864. 10.1073/pnas.0603237103 PubMed DOI PMC

Kotlik, P. , Marková, S. , Horníková, M. , Escalante, M. A. , & Searle, J. B. (2022). The Bank vole (Clethrionomys glareolus) as a model system for adaptive Phylogeography in the European theater. Frontiers in Ecology and Evolution, 10. 10.3389/fevo.2022.866605 DOI

Kryštufek, B. , Tesakov, A. S. , Lebedev, V. S. , Bannikova, A. A. , Abramson, N. I. , & Shenbrot, G. (2020). Back to the future: The proper name for red‐backed voles is Clethrionomys Tilesius and not Myodes Pallas. Mammalia, 84(2), 214–217. 10.1515/mammalia-2019-0067 DOI

Kuwahara, M. , Ise, W. , Ochi, M. , Suzuki, J. , Kometani, K. , Maruyama, S. , Izumoto, M. , Matsumoto, A. , Takemori, N. , Takemori, A. , Shinoda, K. , Nakayama, T. , Ohara, O. , Yasukawa, M. , Sawasaki, T. , Kurosaki, T. , & Yamashita, M. (2016). Bach2–Batf interactions control Th2‐type immune response by regulating the IL‐4 amplification loop. Nature Communications, 7(1), 12596. 10.1038/ncomms12596 PubMed DOI PMC

Laron, Z. (2001). Insulin‐like growth factor 1 (IGF‐1): A growth hormone. Molecular Pathology, 54(5), 311–316. 10.1136/mp.54.5.311 PubMed DOI PMC

Lasky, J. R. , Des Marais, D. L. , McKay, J. K. , Richards, J. H. , Juenger, T. E. , & Keitt, T. H. (2012). Characterizing genomic variation of Arabidopsis thaliana: The roles of geography and climate. Molecular Ecology, 21(22), 5512–5529. 10.1111/j.1365-294X.2012.05709.x PubMed DOI

Lepais, O. , & Weir, J. T. (2014). SimRAD: An R package for simulation‐based prediction of the number of loci expected in RADseq and similar genotyping by sequencing approaches. Molecular Ecology Resources, 14(6), 1314–1321. 10.1111/1755-0998.12273 PubMed DOI

Linnen, C. R. , Kingsley, E. P. , Jensen, J. D. , & Hoekstra, H. E. (2009). On the origin and spread of an adaptive allele in deer mice. Science, 325(5944), 1095–1098. 10.1126/science.1175826 PubMed DOI PMC

Lotterhos, K. E. , & Whitlock, M. C. (2014). Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Molecular Ecology, 23(9), 2178–2192. 10.1111/mec.12725 PubMed DOI PMC

Lovegrove, B. G. (2003). The influence of climate on the basal metabolic rate of small mammals: A slow‐fast metabolic continuum. Journal of Comparative Physiology B, 173(2), 87–112. 10.1007/s00360-002-0309-5 PubMed DOI

Lv, F.‐H. , Agha, S. , Kantanen, J. , Colli, L. , Stucki, S. , Kijas, J. W. , Joost, S. , Li, M.‐H. , & Marsan, P. A. (2014). Adaptations to climate‐mediated selective pressures in sheep. Molecular Biology and Evolution, 31, 3324–3343. 10.1093/molbev/msu264 PubMed DOI PMC

Marková, S. , Horníková, M. , Lanier, H. C. , Henttonen, H. , Searle, J. B. , Weider, L. J. , & Kotlík, P. (2020). High genomic diversity in the bank vole at the northern apex of a range expansion: The role of multiple colonizations and end‐glacial refugia. Molecular Ecology, 29(9), 1730–1744. 10.1111/mec.15427 PubMed DOI

Martin, M. (2011). Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBO Journal, 17(1), 10. 10.14806/ej.17.1.200 DOI

McGrath, J. A. , Stone, K. L. , Begum, R. , Simpson, M. A. , Dopping‐Hepenstal, P. J. , Liu, L. , McMillan, J. R. , South, A. P. , Pourreyron, C. , McLean, W. H. I. , Martinez, A. E. , Mellerio, J. E. , & Parsons, M. (2012). Germline mutation in EXPH5 implicates the Rab27B effector protein Slac2‐b in inherited skin fragility. The American Journal of Human Genetics, 91(6), 1115–1121. 10.1016/j.ajhg.2012.10.012 PubMed DOI PMC

Meirmans, P. G. (2012). The trouble with isolation by distance. Molecular Ecology, 21(12), 2839–2846. 10.1111/j.1365-294X.2012.05578.x PubMed DOI

Micheletti, S. J. , Matala, A. R. , Matala, A. P. , & Narum, S. R. (2018). Landscape features along migratory routes influence adaptive genomic variation in anadromous steelhead (Oncorhynchus mykiss). Molecular Ecology, 27(1), 128–145. 10.1111/mec.14407 PubMed DOI

Murphy, T. L. , Tussiwand, R. , & Murphy, K. M. (2013). Specificity through cooperation: BATF–IRF interactions control immune‐regulatory networks. Nature Reviews Immunology, 13(7), 499–509. 10.1038/nri3470 PubMed DOI

Nachman, M. W. , Hoekstra, H. E. , & D'Agostino, S. L. (2003). The genetic basis of adaptive melanism in pocket mice. Proceedings of the National Academy of Sciences, 100(9), 5268–5273. 10.1073/pnas.0431157100 PubMed DOI PMC

Nadeau, S. , Meirmans, P. G. , Aitken, S. N. , Ritland, K. , & Isabel, N. (2016). The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines. Ecology and Evolution, 6(24), 8649–8664. 10.1002/ece3.2550 PubMed DOI PMC

Nei, M. , & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, 76(10), 5269–5273. 10.1073/pnas.76.10.5269 PubMed DOI PMC

Oue, K. , Zhang, J. , Harada‐Hada, K. , Asano, S. , Yamawaki, Y. , Hayashiuchi, M. , Furusho, H. , Takata, T. , Irifune, M. , Hirata, M. , & Kanematsu, T. (2016). Phospholipase C‐related catalytically inactive protein is a new modulator of thermogenesis promoted by β‐adrenergic receptors in brown adipocytes. Journal of Biological Chemistry, 291(8), 4185–4196. 10.1074/jbc.M115.705723 PubMed DOI PMC

Peterson, B. K. , Weber, J. N. , Kay, E. H. , Fisher, H. S. , & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for De Novo SNP discovery and genotyping in model and non‐model species. PLoS ONE, 7(5), e37135. 10.1371/journal.pone.0037135 PubMed DOI PMC

Phifer‐Rixey, M. , Bi, K. , Ferris, K. G. , Sheehan, M. J. , Lin, D. , Mack, K. L. , Keeble, S. M. , Suzuki, T. A. , Good, J. M. , & Nachman, M. W. (2018). The genomic basis of environmental adaptation in house mice. PLoS Genetics, 14(9), e1007672. 10.1371/journal.pgen.1007672 PubMed DOI PMC

Pörtner, H. (2001). Climate change and temperature‐dependent biogeography: Oxygen limitation of thermal tolerance in animals. Naturwissenschaften, 88(4), 137–146. PubMed

Prates, I. , Penna, A. , Rodrigues, M. T. , & Carnaval, A. C. (2018). Local adaptation in mainland anole lizards: Integrating population history and genome–environment associations. Ecology and Evolution, 8(23), 11932–11944. 10.1002/ece3.4650 PubMed DOI PMC

Pritchard, V. L. , Mäkinen, H. , Vähä, J. P. , Erkinaro, J. , Orell, P. , & Primmer, C. R. (2018). Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence‐related genes. Molecular Ecology, 27(11), 2560–2575. 10.1111/mec.14705 PubMed DOI

R Core Team . (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/

Redeker, S. , Andersen, L. W. , Pertoldi, C. , Madsen, A. B. , Jensen, T. S. , & Jørgensen, J. M. (2006). Genetic structure, habitat fragmentation and bottlenecks in Danish bank voles Clethrionomys glareolus . Mammalian Biology, 71(3), 144–158. 10.1016/j.mambio.2005.12.003 DOI

Rellstab, C. , Gugerli, F. , Eckert, A. J. , Hancock, A. M. , & Holderegger, R. (2015). A practical guide to environmental association analysis in landscape genomics. Molecular Ecology, 24(17), 4348–4370. 10.1111/mec.13322 PubMed DOI

Rezende, E. L. , Bozinovic, F. , Garland, T. , & Garland, T., Jr. (2004). Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution, 58(6), 1361–1374. 10.1111/j.0014-3820.2004.tb01714.x PubMed DOI

Rohfritsch, A. , Galan, M. , Gautier, M. , Gharbi, K. , Olsson, G. E. , Gschloessl, B. , Zeimes, C. , Vanwambeke, S. O. , Vitalis, R. , & Charbonnel, N. (2018). Preliminary insights into the genetics of bank vole tolerance to Puumala hantavirus in Sweden. Ecology and Evolution, 8(22), 11273–11292. 10.1002/ece3.4603 PubMed DOI PMC

Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F‐statistics under isolation by distance. Genetics, 145(4), 1219–1228. PubMed PMC

Sadowska, E. T. , Stawski, C. , Rudolf, A. , Dheyongera, G. , Chrząścik, K. M. , Baliga‐Klimczyk, K. , & Koteja, P. (2015). Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment. Proceedings of the Royal Society B: Biological Sciences, 282(1806), 20150025. 10.1098/rspb.2015.0025 PubMed DOI PMC

Sarkar, A. , Tindle, C. , Pranadinata, R. F. , Reed, S. , Eckmann, L. , Stappenbeck, T. S. , Ernst, P. B. , & Das, S. (2017). ELMO1 regulates autophagy induction and bacterial clearance during enteric infection. The Journal of Infectious Diseases, 216(12), 1655–1666. 10.1093/infdis/jix528 PubMed DOI PMC

Schountz, T. , Acuña‐Retamar, M. , Feinstein, S. , Prescott, J. , Torres‐Perez, F. , Podell, B. , Peters, S. , Ye, C. , Black, W. C. , & Hjelle, B. (2012). Kinetics of immune responses in deer mice experimentally infected with sin Nombre virus. Journal of Virology, 86(18), 10015–10027. 10.1128/jvi.06875-11 PubMed DOI PMC

Schountz, T. , Quackenbush, S. , Rovnak, J. , Haddock, E. , Black, W. C. , Feldmann, H. , & Prescott, J. (2014). Differential lymphocyte and antibody responses in deer mice infected with sin Nombre hantavirus or Andes hantavirus. Journal of Virology, 88(15), 8319–8331. 10.1128/jvi.00004-14 PubMed DOI PMC

Seternes, O.‐M. , Kidger, A. M. , & Keyse, S. M. (2019). Dual‐specificity MAP kinase phosphatases in health and disease. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research, 1866(1), 124–143. 10.1016/j.bbamcr.2018.09.002 PubMed DOI PMC

Sethi, J. K. , & Vidal‐Puig, A. J. (2007). Thematic review series: Adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. Journal of Lipid Research, 48(6), 1253–1262. 10.1194/jlr.R700005-JLR200 PubMed DOI PMC

Sexton, J. P. , Hangartner, S. B. , & Hoffmann, A. A. (2014). Genetic isolation by environment or distance: Which pattern of gene flow is most common? Evolution, 68(1), 1–15. 10.1111/evo.12258 PubMed DOI

Shafer, A. B. A. , & Wolf, J. B. W. (2013). Widespread evidence for incipient ecological speciation: A meta‐analysis of isolation‐by‐ecology. Ecology Letters, 16(7), 940–950. 10.1111/ele.12120 PubMed DOI

Shenbrot, G. I. , & Krasnov, B. R. (2005). Atlas of the geographic distribution of the Arvicoline rodents of the world: Rodentia, Muridae: Arvicoline. Pensoft.

Silver, D. L. , Hou, L. , Somerville, R. , Young, M. E. , Apte, S. S. , & Pavan, W. J. (2008). The secreted metalloprotease ADAMTS20 is required for melanoblast survival. PLoS Genetics, 4(2), e1000003. 10.1371/journal.pgen.1000003 PubMed DOI PMC

Simons, M. J. P. , Reimert, I. , van der Vinne, V. , Hambly, C. , Vaanholt, L. M. , Speakman, J. R. , & Gerkema, M. P. (2011). Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis): A test of the heat dissipation limit theory. Journal of Experimental Biology, 214(1), 38–49. PubMed

Skotte, L. , Korneliussen, T. S. , & Albrechtsen, A. (2013). Estimating individual admixture proportions from next generation sequencing data. Genetics, 195(3), 693–702. 10.1534/genetics.113.154138 PubMed DOI PMC

Söhle, J. , Machuy, N. , Smailbegovic, E. , Holtzmann, U. , Grönniger, E. , Wenck, H. , Stäb, F. , & Winnefeld, M. (2012). Identification of new genes involved in human adipogenesis and fat storage. PLoS One, 7(2), e31193. 10.1371/journal.pone.0031193 PubMed DOI PMC

Stawski, C. , Koteja, P. , & Sadowska, E. T. (2017). A shift in the thermoregulatory curve as a result of selection for high activity‐related aerobic metabolism. Frontiers in Physiology, 8, 1070. 10.3389/fphys.2017.01070 PubMed DOI PMC

Stepanov, V. A. , Kharkov, V. N. , Vagaitseva, K. V. , Bocharova, A. V. , Kazantsev, A. Y. , Popovich, A. A. , & Khitrinskaya, I. Y. (2017). Search for genetic markers of climatic adaptation in populations of North Eurasia. Russian Journal of Genetics, 53(11), 1172–1183. 10.1134/s1022795417110114 DOI

Stillwell, R. C. (2010). Are latitudinal clines in body size adaptive? Oikos, 119(9), 1387–1390. 10.1111/j.1600-0706.2010.18670.x PubMed DOI PMC

Stinchcombe, J. R. , Weinig, C. , Ungerer, M. , Olsen, K. M. , Mays, C. , Halldorsdottir, S. S. , Purugganan, M. D. , & Schmitt, J. (2004). A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences, 101(13), 4712–4717. 10.1073/pnas.0306401101 PubMed DOI PMC

Tarnowska, E. , Niedziałkowska, M. , Gerc, J. , Korbut, Z. , Górny, M. , & Jȩdrzejewska, B. (2016). Spatial distribution of the Carpathian and eastern mtDNA lineages of the bank vole in their contact zone relates to environmental conditions. Biological Journal of the Linnean Society, 119(3), 732–744. 10.1111/bij.12764 DOI

Tiffin, P. , & Ross‐Ibarra, J. (2014). Advances and limits of using population genetics to understand local adaptation. Trends in Ecology & Evolution, 29(12), 673–680. 10.1016/j.tree.2014.10.004 PubMed DOI

Tökölyi, J. , Schmidt, J. , & Barta, Z. (2014). Climate and mammalian life histories. Biological Journal of the Linnean Society, 111(4), 719–736. 10.1111/bij.12238 DOI

Tominaga, K. , Kondo, C. , Kagata, T. , Hishida, T. , Nishizuka, M. , & Imagawa, M. (2004). The novel gene fad158, having a transmembrane domain and leucine‐rich repeat, stimulates adipocyte differentiation. Journal of Biological Chemistry, 279(33), 34840–34848. 10.1074/jbc.M312927200 PubMed DOI

Vasconcelos, L. H. C. , Souza, I. L. L. , Pinheiro, L. S. , & Silva, B. A. (2016). Ion channels in obesity: Pathophysiology and potential therapeutic targets. Frontiers in Pharmacology, 7, 58. 10.3389/fphar.2016.00058 PubMed DOI PMC

Vieira, F. G. , Fumagalli, M. , Albrechtsen, A. , & Nielsen, R. (2013). Estimating inbreeding coefficients from NGS data: Impact on genotype calling and allele frequency estimation. Genome Research, 23(11), 1852–1861. 10.1101/gr.157388.113 PubMed DOI PMC

Viitala, J. , Hakkarainen, H. , & Ylonen, H. (1994). Different dispersal in Clethrionomys and Microtus. Annales Zoologici Fennici, 31(4), 411–415.

Villarino, V. A. , Kanno, Y. , & O'Shea, J. J. (2017). Mechanisms and consequences of Jak–STAT signaling in the immune system. Nature Immunology, 18(4), 374–384. 10.1038/ni.3691 PubMed DOI PMC

Wang, I. J. , & Bradburd, G. S. (2014). Isolation by environment. Molecular Ecology, 23(23), 5649–5662. 10.1111/mec.12938 PubMed DOI

Waterhouse, M. D. , Erb, L. P. , Beever, E. A. , & Russello, M. A. (2018). Adaptive population divergence and directional gene flow across steep elevational gradients in a climate‐sensitive mammal. Molecular Ecology, 27(11), 2512–2528. 10.1111/mec.14701 PubMed DOI

Watterson, G. A. (1975). On the number of segregating sites in genetical models without recombination. Theoretical Population Biology, 7(2), 256–276. 10.1016/0040-5809(75)90020-9 PubMed DOI

Wellenreuther, M. , & Hansson, B. (2016). Detecting polygenic evolution: Problems, pitfalls, and promises. Trends in Genetics, 32(3), 155–164. 10.1016/j.tig.2015.12.004 PubMed DOI

White, T. A. , Perkins, S. E. , Heckel, G. , & Searle, J. B. (2013). Adaptive evolution during an ongoing range expansion: The invasive bank vole (Myodes glareolus) in Ireland. Molecular Ecology, 22(11), 2971–2985. 10.1111/mec.12343 PubMed DOI

Whitlock, M. C. , & Lotterhos, K. E. (2015). Reliable detection of loci responsible for local adaptation: inference of a null model through trimming the distribution of FST. The American Naturalist, 186(S1), S24–S36. 10.1086/682949 PubMed DOI

Wójcik, J. M. , Kawałko, A. , Marková, S. , Searle, J. B. , & Kotlík, P. (2010). Phylogeographic signatures of northward post‐glacial colonization from high‐latitude refugia: A case study of bank voles using museum specimens. Journal of Zoology, 281(4), 249–262. 10.1111/j.1469-7998.2010.00699.x DOI

Wright, S. (1943). Isolation by distance. Genetics, 28(2), 114–138. 10.1093/genetics/28.2.114 PubMed DOI PMC

Xu, B. , & Xie, X. (2016). Neurotrophic factor control of satiety and body weight. Nature Reviews Neuroscience, 17(5), 282–292. 10.1038/nrn.2016.24 PubMed DOI PMC

Yamashita, M. , & Kuwahara, M. (2018). The critical role of Bach2 in regulating type 2 chronic airway inflammation. International Immunology, 30(9), 397–402. 10.1093/intimm/dxy020 PubMed DOI

Yamawaki, Y. , Oue, K. , Shirawachi, S. , Asano, S. , Harada, K. , & Kanematsu, T. (2017). Phospholipase C‐related catalytically inactive protein can regulate obesity, a state of peripheral inflammation. Japanese Dental Science Review, 53(1), 18–24. 10.1016/j.jdsr.2016.06.001 PubMed DOI PMC

Yeaman, S. (2015). Local adaptation by alleles of small effect. American Naturalist, 186(S1), S74–S89. 10.1086/682405 PubMed DOI

Yudin, N. S. , Larkin, D. M. , & Ignatieva, E. V. (2017). A compendium and functional characterization of mammalian genes involved in adaptation to Arctic or Antarctic environments. BMC Genetics, 18(S1), 111. 10.1186/s12863-017-0580-9 PubMed DOI PMC

Zhang, Y. , Blattman, J. N. , Kennedy, N. J. , Duong, J. , Nguyen, T. , Wang, Y. , Davis, R. J. , Greenberg, P. D. , Flavell, R. A. , & Dong, C. (2004). Regulation of innate and adaptive immune responses by MAP kinase phosphatase 5. Nature, 430(7001), 793–797. 10.1038/nature02764 PubMed DOI

Zhang, Y. , Yue, J. , Che, H. , Sun, H. , Tse, H. , & Li, G. (2013). BKCa and hEag1 channels regulate cell proliferation and differentiation in human bone marrow‐derived mesenchymal stem cells. Journal of Cellular Physiology, 229(2), 202–212. 10.1002/jcp.24435 PubMed DOI

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