Current species distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene-Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence from one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10 000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original postglacial colonists (the northern cluster) was probably replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasizes the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.

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

Evolutionary Biology Group Faculty of Biology Adam Mickiewicz University Poznan Poland

Institute of Environmental Sciences Jagiellonian University Gronostajowa 7 30 387 Krakow Poland

Laboratory of Molecular Ecology Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Rumburská 89 277 21 Liběchov Czech Republic

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Hewitt GM. 2000. The genetic legacy of the quaternary ice ages. Nature 405, 907–913. (10.1038/35016000) PubMed DOI

Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson J-F. 1998. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464. (10.1046/j.1365-294x.1998.00289.x) PubMed DOI

Hewitt GM. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58, 247–276. (10.1111/j.1095-8312.1996.tb01434.x) DOI

Searle JB, Kotlík P, Rambau RV, Marková S, Herman JS, McDevitt AD. 2009. The Celtic fringe of Britain: insights from small mammal phylogeography. Proc. R. Soc. B 276, 4287–4294. (10.1098/rspb.2009.1422) PubMed DOI PMC

Brace S, Ruddy M, Miller R, Schreve DC, Stewart JR, Barnes I. 2016. The colonization history of British water vole (Arvicola amphibius (Linnaeus, 1758)): origins and development of the Celtic fringe. Proc. R. Soc. B 283, 20160130 (10.1098/rspb.2016.0130) PubMed DOI PMC

Montgomery WI, Provan J, McCabe AM, Yalden DW. 2014. Origin of British and Irish mammals: disparate post-glacial colonisation and species introductions. Quat. Sci. Rev. 98, 144–165. (10.1016/j.quascirev.2014.05.026) DOI

Piertney SB, Stewart WA, Lambin X, Telfer S, Aars J, Dallas JF. 2005. Phylogeographic structure and postglacial evolutionary history of water voles (Arvicola terrestris) in the United Kingdom. Mol. Ecol. 14, 1435–1444. (10.1111/j.1365-294X.2005.02496.x) PubMed DOI

Barnes I, Matheus P, Shapiro B, Jensen D, Cooper A. 2002. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science 295, 2267–2270. (10.1126/science.1067814) PubMed DOI

Pergams ORW, Barnes WM, Nyberg D. 2003. Rapid change in mouse mitochondrial DNA. Nature 423, 397 (10.1038/423397a) PubMed DOI

Dalen L, et al. 2012. Partial genetic turnover in Neandertals: continuity in the east and population replacement in the west. Mol. Biol. Evol. 29, 1893–1897. (10.1093/molbev/mss074) PubMed DOI

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

Hall SJG. 1979. Haemoglobin polymorphism in the bank vole, Clethrionomys glareolus, in Britain. J. Zool. 187, 153–160. (10.1111/j.1469-7998.1979.tb03939.x) DOI

Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664. (10.1101/gr.094052.109) PubMed DOI PMC

Pickrell JK, et al. 2012. The genetic prehistory of southern Africa. Nat. Commun. 3, 1143 (10.1038/ncomms2140) PubMed DOI PMC

Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (10.1371/journal.pgen.1002967) PubMed DOI PMC

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

Marková S, Searle JB, Kotlík P. 2014. Relaxed functional constraints on triplicate alpha-globin gene in the bank vole suggest a different evolutionary history from other rodents. Heredity 113, 64–73. (10.1038/hdy.2014.12) PubMed DOI PMC

Cox MP, Peterson DA, Biggs PJ. 2010. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11, 485 (10.1186/1471-2105-11-485) PubMed DOI PMC

Martin M. 2012. Cutadapt removes adapter sequences from high-throughput sequencing reads. Bioinformatics Action 17, 10–12.

Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652. (10.1038/nbt.1883) PubMed DOI PMC

Stuglik MT, Babik W, Prokop Z, Radwan J. 2014. Alternative reproductive tactics and sex-biased gene expression: the study of the bulb mite transcriptome. Ecol. Evol. 4, 623–632. (10.1002/ece3.965) DOI

Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. (10.1038/nmeth.1923) PubMed DOI PMC

Li H, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079. (10.1093/bioinformatics/btp352) PubMed DOI PMC

Foll M, Gaggiotti O. 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993. (10.1534/genetics.108.092221) PubMed DOI PMC

Wigginton JE, Cutler DJ, Abecasis GR. 2005. A note on exact tests of Hardy-Weinberg equilibrium. Am. J. Hum. Genet. 76, 887–893. (10.1086/429864) PubMed DOI PMC

Martins H, Caye K, Luu K, Blum MG, Francois O. 2016. Identifying outlier loci in admixed and in continuous populations using ancestral population differentiation statistics. Mol. Ecol. 25, 5029–5042. (10.1111/mec.13822) PubMed DOI

Danecek P, et al. 2011. The variant call format and VCFtools. Bioinformatics 27, 2156–2158. (10.1093/bioinformatics/btr330) PubMed DOI PMC

Purcell S, et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575. (10.1086/519795) PubMed DOI PMC

Kotlík P, Marková S, Konczal M, Babik W, Searle JB.2018. Data from: Genomics of end-Pleistocene population replacement in a small mammal. Dryad Digital Repository. ( ) PubMed DOI PMC

Excoffier L, Lischer HE. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10, 564–567. (10.1111/j.1755-0998.2010.02847.x) PubMed DOI

Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2, e190 (10.1371/journal.pgen.0020190) PubMed DOI PMC

Alexander DH, Lange K. 2011. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12, 246 (10.1186/1471-2105-12-246) PubMed DOI PMC

Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959. PubMed PMC

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620. (10.1111/j.1365-294X.2005.02553.x) PubMed DOI

Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, Guillemaud T, Estoup A. 2008. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24, 2713–2719. (10.1093/bioinformatics/btn514) PubMed DOI PMC

Bertorelle G, Benazzo A, Mona S. 2010. ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol. Ecol. 19, 2609–2625. (10.1111/j.1365-294X.2010.04690.x) PubMed DOI

Csillery K, Blum MG, Gaggiotti OE, Francois O. 2010. Approximate Bayesian Computation (ABC) in practice. Trends Ecol. Evol. 25, 410–418. (10.1016/j.tree.2010.04.001) PubMed DOI

Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, Estoup A. 2014. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189. (10.1093/bioinformatics/btt763) PubMed DOI

Hanselmann M, Kothe U, Kirchner M, Renard BY, Amstalden ER, Glunde K, Heeren RM, Hamprecht FA. 2009. Toward digital staining using imaging mass spectrometry and random forests. J. Proteome Res. 8, 3558–3567. (10.1021/pr900253y) PubMed DOI PMC

Pudlo P, Marin JM, Estoup A, Cornuet JM, Gautier M, Robert CP. 2016. Reliable ABC model choice via random forests. Bioinformatics 32, 859–866. (10.1093/bioinformatics/btv684) PubMed DOI

Fraimout A, et al. 2017. Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Mol. Biol. Evol. 34, 980–996. PubMed PMC

Momigliano P, Jokinen H, Fraimout A, Florin AB, Norkko A, Merila J. 2017. Extraordinarily rapid speciation in a marine fish. Proc. Natl Acad. Sci. USA 114, 6074–6079. (10.1073/pnas.1615109114) PubMed DOI PMC

Strobl C, Malley J, Tutz G. 2009. An introduction to recursive partitioning: rationale, application, and characteristics of classification and regression trees, bagging, and random forests. Psychol. Methods 14, 323–348. (10.1037/a0016973) PubMed DOI PMC

Novembre J, Stephens M. 2008. Interpreting principal component analyses of spatial population genetic variation. Nat. Genet. 40, 646–649. (10.1038/ng.139) PubMed DOI PMC

McVean G. 2009. A genealogical interpretation of principal components analysis. PLoS Genet. 5, e1000686 (10.1371/journal.pgen.1000686) PubMed DOI PMC

Ryabokon NI, Goncharova RI. 2006. Transgenerational accumulation of radiation damage in small mammals chronically exposed to Chernobyl fallout. Radiat. Environ. Biophys. 45, 167–177. (10.1007/s00411-006-0054-3) PubMed DOI

Buggs RJ. 2007. Empirical study of hybrid zone movement. Heredity 99, 301–312. (10.1038/sj.hdy.6800997) PubMed DOI

Shaw DD, Wilkinson P, Moran C. 1979. A comparison of chromosomal and allozymal variation across a narrow hybrid zone in the grasshopper Caledia captiva. Chromosoma 75, 333–351. (10.1007/BF00293476) PubMed DOI

Berg JJ, Coop G. 2014. A population genetic signal of polygenic adaptation. PLoS Genet. 10, e1004412 (10.1371/journal.pgen.1004412) PubMed DOI PMC

Atkins KE, Travis JM. 2010. Local adaptation and the evolution of species' ranges under climate change. J. Theor. Biol. 266, 449–457. (10.1016/j.jtbi.2010.07.014) PubMed DOI

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