Increasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous β-globin genes of the bank vole (Clethrionomys glareolus) in Britain in which the ancestral serine (Ser) and the derived cysteine (Cys) allele represent geographically partitioned functional variation affecting the erythrocyte antioxidative capacity. Here we studied the geographical pattern of the two-locus Ser/Cys polymorphism throughout Europe and tested for the geographic correlation between environmental variables and allele frequency, expected if the polymorphism was under spatially heterogeneous environment-related selection. Although bank vole population history clearly is important in shaping the dispersal of the oxidative stress protective Cys allele, analyses correcting for population structure suggest the Europe-wide pattern is affected by geographical variation in environmental conditions. The β-globin phenotype is encoded by the major paralog HBB-T1 but we found evidence of bidirectional gene conversion of exon 2 with the low-expression paralog HBB-T2. Our data support the model where gene conversion reshuffling genotypes between high- and low- expressed paralogs enables tuning of erythrocyte thiol levels, which may help maintain intracellular redox balance under fluctuating environmental conditions. Therefore, our study suggests a possible role for gene conversion between differentially expressed gene duplicates as a mechanism of physiological adaptation of populations to new or changing environments.

Department of Animal Science and Food Processing Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Kamýcká 129 165 00 Prague 6 Suchdol Czech Republic

Department of Ecology and Evolutionary Biology Cornell University Ithaca NY 14853 USA

Department of Zoology Faculty of Science Charles University Viničná 7 12844 Prague 2 Czech Republic

Laboratory of Molecular Ecology Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 27721 Liběchov Czech Republic

Zobrazit více v PubMed

Bergland A.O., Behrman E.L., O’Brien K.R., Schmidt P.S., Petrov D.A. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 2014;10:e1004775. doi: 10.1371/journal.pgen.1004775. PubMed DOI PMC

de Filippo C., Key F.M., Ghirotto S., Benazzo A., Meneu J.R., Weihmann A., NISC Comparative Sequence Program. Parra G., Green E.D., Andrés A.M. Recent selection changes in human genes under long-term balancing selection. Mol. Biol. Evol. 2016;33:1435–1447. doi: 10.1093/molbev/msw023. PubMed DOI PMC

Hermisson J., Pennings P.S. Soft sweeps and beyond: Understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol. Evol. 2017;8:700–716. doi: 10.1111/2041-210X.12808. DOI

Llaurens V., Whibley A., Joron M. Genetic architecture and balancing selection: The life and death of differentiated variants. Mol. Ecol. 2017;26:2430–2448. doi: 10.1111/mec.14051. PubMed DOI

Mackinnon M.J., Ndila C., Uyoga S., Macharia A., Snow R.W., Band G., Rautanen A., Rockett K.A., Kwiatkowski D.P., Williams T.N. Environmental correlation analysis for genes associated with protection against malaria. Mol. Biol. Evol. 2016;33:1188–1204. doi: 10.1093/molbev/msw004. PubMed DOI PMC

Gagnaire P.-A., Normandeau E., Côté C., Hansen M.M., Bernatchez L. The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata) Genetics. 2012;190:725–736. doi: 10.1534/genetics.111.134825. PubMed DOI PMC

Hermisson J., Pennings P.S. Soft sweeps: Molecular population genetics of adaptation from standing genetic variation. Genetics. 2005;169:2335–2352. doi: 10.1534/genetics.104.036947. PubMed DOI PMC

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

Pelz H.-J., Rost S., Hünerberg M., Fregin A., Heiberg A.-C., Baert K., MacNicoll A.D., Prescott C.V., Walker A.-S., Oldenburg J., et al. The genetic basis of resistance to anticoagulants in rodents. Genetics. 2005;170:1839–1847. doi: 10.1534/genetics.104.040360. PubMed DOI PMC

Steiner C.C., Weber J.N., Hoekstra H.E. Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol. 2007;5:e219. doi: 10.1371/journal.pbio.0050219. PubMed DOI PMC

Liu S., Lorenzen E.D., Fumagalli M., Li B., Harris K., Xiong Z., Zhou L., Korneliussen T.S., Somel M., Babbitt C., et al. Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell. 2014;157:785–794. doi: 10.1016/j.cell.2014.03.054. PubMed DOI PMC

Bataillon T., Galtier N., Bernard A., Cryer N., Faivre N., Santoni S., Severac D., Mikkelsen T.N., Larsen K.S., Beier C., et al. A replicated climate change field experiment reveals rapid evolutionary response in an ecologically important soil invertebrate. Glob. Chang. Biol. 2016;22:2370–2379. doi: 10.1111/gcb.13293. PubMed DOI PMC

Weber R.E., Ostojic H., Fago A., Dewilde S., Van Hauwaert M.-L., Moens L., Monge C. Novel mechanism for high-altitude adaptation in hemoglobin of the Andean frog Telmatobius peruvianus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002;283:R1052–R1060. doi: 10.1152/ajpregu.00292.2002. PubMed DOI

Storz J.F., Sabatino S.J., Hoffmann F.G., Gering E.J., Moriyama H., Ferrand N., Monteiro B., Nachman M.W. The molecular basis of high-altitude adaptation in deer mice. PLoS Genet. 2007;3:e45. doi: 10.1371/journal.pgen.0030045. PubMed DOI PMC

Storz J.F., Runck A.M., Sabatino S.J., Kelly J.K., Ferrand N., Moriyama H., Weber R.E., Fago A. Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proc. Natl. Acad. Sci. USA. 2009;106:14450–14455. doi: 10.1073/pnas.0905224106. PubMed DOI PMC

McCracken K.G., Barger C.P., Bulgarella M., Johnson K.P., Sonsthagen S.A., Trucco J., Valqui T.H., Wilson R.E., Winker K., Sorenson M.D. Parallel evolution in the major haemoglobin genes of eight species of Andean waterfowl. Mol. Ecol. 2009;18:3992–4005. doi: 10.1111/j.1365-294X.2009.04352.x. PubMed DOI

McCracken K.G., Barger C.P., Bulgarella M., Johnson K.P., Kuhner M.K., Moore A.V., Peters J.L., Trucco J., Valqui T.H., Winker K., et al. Signatures of high-altitude adaptation in the major hemoglobin of five species of Andean dabbling ducks. Am. Nat. 2009;174:631–650. doi: 10.1086/606020. PubMed DOI

Campbell K.L., Storz J.F., Signore A.V., Moriyama H., Catania K.C., Payson A.P., Bonaventura J., Stetefeld J., Weber R.E. Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole. BMC Evol. Biol. 2010;10:214. doi: 10.1186/1471-2148-10-214. PubMed DOI PMC

Campbell K.L., Roberts J.E.E., Watson L.N., Stetefeld J., Sloan A.M., Signore A.V., Howatt J.W., Tame J.R.H., Rohland N., Shen T.-J., et al. Substitutions in woolly mammoth hemoglobin confer biochemical properties adaptive for cold tolerance. Nat. Genet. 2010;42:536–540. doi: 10.1038/ng.574. PubMed DOI

Natarajan C., Hoffmann F.G., Lanier H.C., Wolf C.J., Cheviron Z.A., Spangler M.L., Weber R.E., Fago A., Storz J.F. Intraspecific polymorphism, interspecific divergence, and the origins of function-altering mutations in deer mouse hemoglobin. Mol. Biol. Evol. 2015;32:978–997. doi: 10.1093/molbev/msu403. PubMed DOI PMC

Di Simplicio P., Cacace M.G., Lusini L., Giannerini F., Giustarini D., Rossi R. Role of protein -SH groups in redox homeostasis—The erythrocyte as a model system. Arch. Biochem. Biophys. 1998;355:145–152. doi: 10.1006/abbi.1998.0694. PubMed DOI

Giustarini D., Dalle-Donne I., Cavarra E., Fineschi S., Lungarella G., Milzani A., Rossi R. Metabolism of oxidants by blood from different mouse strains. Biochem. Pharmacol. 2006;71:1753–1764. doi: 10.1016/j.bcp.2006.03.015. PubMed DOI

Storz J.F., Weber R.E., Fago A. Oxygenation properties and oxidation rates of mouse hemoglobins that differ in reactive cysteine content. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2012;161:265–270. doi: 10.1016/j.cbpa.2011.11.004. PubMed DOI PMC

Vitturi D.A., Sun C.-W., Harper V.M., Thrash-Williams B., Cantu-Medellin N., Chacko B.K., Peng N., Dai Y., Wyss J.M., Townes T., et al. Antioxidant functions for the hemoglobin β93 cysteine residue in erythrocytes and in the vascular compartment in vivo. Free Radic. Biol. Med. 2013;55:119–129. doi: 10.1016/j.freeradbiomed.2012.11.003. PubMed DOI PMC

Kotlík P., Marková S., Vojtek L., Stratil A., Šlechta V., Hyršl P., Searle J.B. Adaptive phylogeography: Functional divergence between haemoglobins derived from different glacial refugia in the bank vole. Proc. R. Soc. B. 2014;281:20140021. doi: 10.1098/rspb.2014.0021. PubMed DOI PMC

Hall S.J.G. Haemoglobin polymorphism in the bank vole, Clethrionomys glareolus, in Britain. J. Zool. 1979;187:153–160. doi: 10.1111/j.1469-7998.1979.tb03939.x. DOI

Rossi R., Barra D., Bellelli A., Boumis G., Canofeni S., Di Simplicio P., Lusini L., Pascarella S., Amiconi G. Fast-reacting thiols in rat hemoglobins can intercept damaging species in erythrocytes more efficiently than glutathione. J. Biol. Chem. 1998;273:19198–19206. doi: 10.1074/jbc.273.30.19198. PubMed DOI

Miranda J.J. Highly reactive cysteine residues in rodent hemoglobins. Biochem. Biophys. Res. Commun. 2000;275:517–523. doi: 10.1006/bbrc.2000.3326. PubMed DOI

Pörtner H.O. Physiological basis of temperature-dependent biogeography: Trade-offs in muscle design and performance in polar ectotherms. J. Exp. Biol. 2002;205:2217–2230. PubMed

Losdat S., Helfenstein F., Blount J.D., Richner H. Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird. J. Evol. Biol. 2014;27:1990–2000. doi: 10.1111/jeb.12454. PubMed DOI

Novembre J., Di Rienzo A. Spatial patterns of variation due to natural selection in humans. Nat. Rev. Genet. 2009;10:745–755. doi: 10.1038/nrg2632. PubMed DOI PMC

Manel S., Conord C., Després L. Genome scan to assess the respective role of host-plant and environmental constraints on the adaptation of a widespread insect. BMC Evol. Biol. 2009;9:288. doi: 10.1186/1471-2148-9-288. PubMed DOI PMC

Stucki S., Orozco-terWengel P., Forester B.R., Duruz S., Colli L., Masembe C., Negrini R., Landguth E., Jones M.R., The NEXTGEN Consortium et al. High performance computation of landscape genomic models including local indicators of spatial association. Mol. Ecol. Resour. 2016;17:1072–1089. doi: 10.1111/1755-0998.12629. PubMed DOI

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

Kotlík P., Deffontaine V., Mascheretti S., Zima J., Michaux J.R., Searle J.B. A northern glacial refugium for bank voles (Clethrionomys glareolus) Proc. Natl. Acad. Sci. USA. 2006;103:14860–14864. doi: 10.1073/pnas.0603237103. PubMed DOI PMC

Filipi K., Marková S., Searle J.B., Kotlík P. Mitogenomic phylogenetics of the bank vole (Clethrionomys glareolus), a model system for studying end-glacial colonization of Europe. Mol. Phylogenet. Evol. 2015;82:245–257. doi: 10.1016/j.ympev.2014.10.016. PubMed DOI

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

Runck A.M., Weber R.E., Fago A., Storz J.F. Evolutionary and functional properties of a two-locus β-globin polymorphism in Indian house mice. Genetics. 2010;184:1121–1131. doi: 10.1534/genetics.109.113506. PubMed DOI PMC

Storz J.F., Natarajan C., Cheviron Z.A., Hoffmann F.G., Kelly J.K. Altitudinal variation at duplicated β-globin genes in deer mice: Effects of selection, recombination, and gene conversion. Genetics. 2012;190:203–216. doi: 10.1534/genetics.111.134494. PubMed DOI PMC

Rousset F. Genepop’007: A complete re-implementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 2008;8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x. PubMed DOI

Stephens M., Smith N.J., Donnelly P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 2001;68:978–989. doi: 10.1086/319501. PubMed DOI PMC

Stephens M., Donnelly P. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 2003;73:1162–1169. doi: 10.1086/379378. PubMed DOI PMC

Librado P., Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI

Haldane J.B.S. An exact test for randomness of mating. J. Genet. 1954;52:631–635. doi: 10.1007/BF02985085. DOI

Rousset F., Raymond M. Testing heterozygote excess and deficiency. Genetics. 1995;140:1413–1419. PubMed PMC

Asmussen M.A., Basten C.J. Constraints and normalized measures for cytonuclear disequilibria. Heredity. 1996;76:207–214. doi: 10.1038/hdy.1996.33. PubMed DOI

Basten C.J., Asmussen M.A. The exact test for cytonuclear disequilibria. Genetics. 1997;146:1165–1171. PubMed PMC

Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 2005;25:1965–1978. doi: 10.1002/joc.1276. DOI

Stuart P., Mirimin L., Cross T.F., Sleeman D.P., Buckley N.J., Telfer S., Birtles R.J., Kotlík P., Searle J.B. The origin of Irish bank voles (Clethrionomys glareolus) assessed by mitochondrial DNA analysis. Ir. Nat. J. 2007;28:440–446.

Joost S., Bonin A., Bruford M.W., Després L., Conord C., Erhardt G., Taberlet P. A spatial analysis method (SAM) to detect candidate loci for selection: Towards a landscape genomics approach to adaptation. Mol. Ecol. 2007;16:3955–3969. doi: 10.1111/j.1365-294X.2007.03442.x. PubMed DOI

Pond S.L.K., Frost S.D. Datamonkey: Rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005;21:2531–2533. doi: 10.1093/bioinformatics/bti320. PubMed DOI

Pond S.L.K., Muse S.V. HyPhy: Hypothesis Testing Using Phylogenies. In: Nielsen R., editor. Statistical Methods in Molecular Evolution. Springer; New York, NY, USA: 2005. pp. 125–181.

Pond S.L.K., Posada D., Gravenor M.B., Woelk C.H., Frost S.D. Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol. 2006;23:1891–1901. doi: 10.1093/molbev/msl051. PubMed DOI

Pond S.L.K., Posada D., Gravenor M.B., Woelk C.H., Frost S.D. GARD: A genetic algorithm for recombination detection. Bioinformatics. 2006;22:3096–3098. doi: 10.1093/bioinformatics/btl474. PubMed DOI

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Betrán E., Rozas J., Navarro A., Barbadilla A. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics. 1997;146:89–99. PubMed PMC

Sawyer S. Statistical tests for detecting gene conversion. Mol. Biol. Evol. 1989;6:526–538. doi: 10.1093/oxfordjournals.molbev.a040567. PubMed DOI

Sawyer S. GENECONV: A Computer Package for The Statistical Detection of Gene Conversion. Department of Mathematics, Washington University in St. Louis; St. Louis, MO, USA: 1999.

Storz J.F., Baze M., Waite J.L., Hoffmann F.G., Opazo J.C., Hayes J.P. Complex signatures of selection and gene conversion in the duplicated globin genes of house mice. Genetics. 2007;177:481–500. doi: 10.1534/genetics.107.078550. PubMed DOI PMC

Nei M. Molecular Evolutionary Genetics. Columbia University Press; New York, NY, USA: 1987.

Prevodnik A., Gardestrom J., Lilja K., Elfwing T., McDonagh B., Petrovic N., Tedengren M., Sheehan D., Bollner T. Oxidative stress in response to xenobiotics in the blue mussel Mytilus edulis L.: Evidence for variation along a natural salinity gradient of the Baltic Sea. Aquat. Toxicol. 2007;82:63–71. doi: 10.1016/j.aquatox.2007.01.006. PubMed DOI

Costantini D., Dell’Omo G., De Filippis S.P., Marquez C., Snell H.L., Snell H.M., Tapia W., Brambilla G., Gentile G. Temporal and spatial covariation of gender and oxidative stress in the Galápagos land iguana Conolophus subcristatus. Physiol. Biochem. Zool. 2009;82:430–437. doi: 10.1086/604668. PubMed DOI

Searle J.B., Kotlík P., Rambau R.V., Marková S., Herman J.S., McDevitt A.D. The Celtic fringe of Britain: Insights from small mammal phylogeography. Proc. R. Soc. Lond. B. 2009;276:4287–4294. doi: 10.1098/rspb.2009.1422. PubMed DOI PMC

Frichot E., Schoville S.D., de Villemereuil P., Gaggiotti O.E., François O. Detecting adaptive evolution based on association with ecological gradients: Orientation matters! Heredity. 2015;115:22. doi: 10.1038/hdy.2015.7. PubMed DOI PMC

Stier A., Dupoué A., Picard D., Angelier F., Brischoux F., Lourdais O. Oxidative stress in a capital breeder (Vipera aspis) facing pregnancy and water constraints. J. Exp. Biol. 2017;220:1792–1796. doi: 10.1242/jeb.156752. PubMed DOI

Lee C., Mitchell-Olds T. Environmental adaptation contributes to gene polymorphism across the Arabidopsis thaliana genome. Mol. Biol. Evol. 2012;29:3721–3728. doi: 10.1093/molbev/mss174. PubMed DOI PMC

Tiffin P., Ross-Ibarra J. Advances and limits of using population genetics to understand local adaptation. Trends Ecol. Evol. 2014;29:673–680. doi: 10.1016/j.tree.2014.10.004. PubMed DOI

Outridge P.M., Hutchinson T.C. Induction of cadmium tolerance by acclimation transferred between ramets of the clonal fern Salvinia minima Baker. New Phytol. 1991;117:597–605. doi: 10.1111/j.1469-8137.1991.tb00964.x. DOI

Marino S.M., Gladyshev V.N. Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J. Mol. Biol. 2010;404:902–916. doi: 10.1016/j.jmb.2010.09.027. PubMed DOI PMC

Mano S., Innan H. The evolutionary rate of duplicated genes under concerted evolution. Genetics. 2008;180:493–505. doi: 10.1534/genetics.108.087676. PubMed DOI PMC

Hallast P., Nagirnaja L., Margus T., Laan M. Segmental duplications and gene conversion: Human luteinizing hormone/chorionic gonadotropin β gene cluster. Genome Res. 2005;15:1535–1546. doi: 10.1101/gr.4270505. PubMed DOI PMC

von Salomé J., Kukkonen J.P. Sequence features of HLA-DRB1 locus define putative basis for gene conversion and point mutations. BMC Genom. 2008;9:228. doi: 10.1186/1471-2164-9-228. PubMed DOI PMC

Lam S.T., Stahl M.M., McMilin K.D., Stahl F.W. Rec-mediated recombinational hot spot activity in bacteriophage lambda. II. A mutation which causes hot spot activity. Genetics. 1974;77:425–433. PubMed PMC

Henderson D., Weil J. Recombination-deficient deletions in bacteriophage lambda and their interaction with chi mutations. Genetics. 1975;79:143–174. PubMed PMC

Smith G.R. How RecBCD enzyme and Chi promote DNA break repair and recombination: A molecular biologist’s view. Microbiol. Mol. Biol. Rev. 2012;76:217–228. doi: 10.1128/MMBR.05026-11. PubMed DOI PMC

Kenter A.L., Birshtein B.K. Chi, a promoter of generalized recombination in λ phage, is present in immunoglobulin genes. Nature. 1981;293:402–404. doi: 10.1038/293402a0. PubMed DOI

Matsuno Y., Yamashiro Y., Yamamoto K., Hattori Y., Yamamoto K., Ohba Y., Miyaji T. A possible example of gene conversion with a common β-thalassemia mutation and Chi sequence present in the β-globin gene. Hum. Genet. 1992;88:357–358. doi: 10.1007/BF00197277. PubMed DOI

Chen J.-M., Ferec C. Gene conversion-like missense mutations in the human cationic trypsinogen gene and insights into the molecular evolution of the human trypsinogen family. Mol. Genet. Metab. 2000;71:463–469. doi: 10.1006/mgme.2000.3086. PubMed DOI

López-Correa C., Dorschner M., Brems H., Lázaro C., Clementi M., Upadhyaya M., Dooijes D., Moog U., Kehrer-Sawatzki H., Rutkowski J.L., et al. Recombination hotspot in NF1 microdeletion patients. Hum. Mol. Genet. 2001;10:1387–1392. doi: 10.1093/hmg/10.13.1387. PubMed DOI

Zhang W., Cai W.-W., Zhou W.-P., Li H.-P., Li L., Yan W., Deng Q.-K., Zhang Y.-P., Fu Y.-X., Xu X.-M. Evidence of gene conversion in the evolutionary process of the codon 41/42 (-CTTT) mutation causing β-thalassemia in southern China. J. Mol. Evol. 2008;66:436–445. doi: 10.1007/s00239-008-9096-2. PubMed DOI

Innan H. A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes. Proc. Natl. Acad. Sci. USA. 2003;100:8793–8798. doi: 10.1073/pnas.1031592100. PubMed DOI PMC

Lafontaine G., Napier J.D., Petit R.J., Hu F.S. Invoking adaptation to decipher the genetic legacy of past climate change. Ecology. 2018;99:1530–1546. doi: 10.1002/ecy.2382. PubMed DOI

Genetic admixture drives climate adaptation in the bank vole

Genic distribution modelling predicts adaptation of the bank vole to climate change

A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole

Niche differentiation in a postglacial colonizer, the bank vole Clethrionomys glareolus