Pleistocene glaciations had significant effects on the distribution and evolution of species inhabiting the Holarctic region. Phylogeographic studies concerning the entire region are still rare. Here, we compared global phylogeographic patterns of one boreo-montane and one boreo-temperate butterflies with largely overlapping distribution ranges across the Northern Hemisphere, but with different levels of range fragmentation and food specialization. We reconstructed the global phylogeographic history of the boreo-montane specialist Boloria eunomia (n = 223) and of the boreo-temperate generalist Boloria selene (n = 106) based on mitochondrial and nuclear DNA markers, and with species distribution modelling (SDM). According to the genetic structures obtained, both species show a Siberian origin and considerable split among populations from Nearctic and Palaearctic regions. According to SDMs and molecular data, both butterflies could inhabit vast areas during the moderate glacials. In the case of B. selene, high haplotype diversity and low geographic structure suggest long-lasting interconnected gene flow among populations. A stronger geographic structuring between populations was identified in the specialist B. eunomia, presumably due to the less widespread, heterogeneously distributed food resources, associated with cooler and more humid climatic conditions. Populations of both species show opposite patterns across major parts of North America and in the case of B. eunomia also across Asia. Our data underline the relevance to cover entire distribution ranges to reconstruct the correct phylogeographic history of species.

Biology Centre of the Czech Academy of Sciences Institute of Entomology Ceske Budejovice Czech Republic

IMBE Aix Marseille Université CNRS IRD Avignon Université Marseille France

Laboratory of Insect Evolutionary Biology and Ecology Institute of Biology University of Białystok Białystok Poland

Terrestrial Ecology Research Group Department of Ecology and Ecosystem Management School of Life Sciences Weihenstephan Technische Universität München Freising Germany

University of South Bohemia Faculty of Sciences Ceske Budejovice Czech Republic

Zobrazit více v PubMed

Avise JC. Phylogeography—the history and formation of species. Cambridge, Massachusetts, London: Harvard University Press; 2000.

Hewitt GM. The structure of biodiversity—insights from molecular phylogeography. Front Zool. 2004;1:4 10.1186/1742-9994-1-4 PubMed DOI PMC

Hewitt GM. Post-glacial re-colonization of European biota. Biol J Linn Soc Lond. 1999;68:87–112.

Seddon JM, Santucci F, Reeve NJ, Hewitt GM. DNA footprints of European hedgehogs, PubMed

Varga Z, Schmitt T. Types of areal and oreotundral disjunctions in the western Palearctic. Biol J Linn Soc Lond. 2008;93:415–430.

Ronikier M, Schneeweiss GM, Schoönswetter P. The extreme disjunction between Beringia and Europe in PubMed DOI

Schmitt T, Varga Z. Extra-Mediterranean refugia: The rule and not the exception? Front Zool. 2012;9:22 10.1186/1742-9994-9-22 PubMed DOI PMC

de Lattin G. Grundriss der Zoogeographie. Fischer, Stuttgart: Fischer; 1967.

Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool. 2007;4:11 10.1186/1742-9994-4-11 PubMed DOI PMC

Després L, Loriot S, Gaudeul M. Geographic pattern of genetic variation in the European globeflower PubMed

Kramp K, Huck S, Niketić M, Tomović G, Schmitt T. Multiple glacial refugia and complex postglacial range shifts of the obligatory woodland plant PubMed

Drees C, Husemann M, Homburg K, Brandt P, Dieker P, Habel JC, et al. Molecular analyses and species distribution models indicate cryptic northern mountain refugia for a forest-dwelling ground beetle. J Biogeogr. 2016;43:2223–2236.

Habel JCH, Schmitt T, Meyer M, Finger A, Rödder D, Assmann T, et al. Biogeography meets conservation: the genetic structure of the endangered lycaenid butterfly

Kramp K, Cizek O, Madeira PM, Ramos AA, Konvicka M, Castilho R, et al. Genetic implications of phylogeographical patterns in the conservation of the boreal wetland butterfly

Nève G, Barascud B, Hughes R, Aubert J, Descimon H, Lebrun P, et al. Dispersal, colonization power and metapopulation structure in the vulnerable butterfly

Binney HA, Willis KJ, Edwards ME, Bhagwat SA, Anderson PM, Andreev AA, et al. The distribution of late-Quaternary woody taxa in northern Eurasia: evidence from a new macrofossil database. Quat Sci Rev. 2009;28:2445–2464.

Ehlers J, Gibbard PL. The extent and chronology of Cenozoic global glaciation. Quat Int 2007;164:6–20.

Tarasov PE, Volkova VS, Webb T III, Guiot J, Andreev AA, Bezusko LG, et al. Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. J Biogeogr. 2000;27:609–620.

Abbott RJ, Brochmann C. History and evolution of the Arctic flora: in the footsteps of Eric Hultén. Mol Ecol. 2003;12:299–313. PubMed

Goetcheus VG, Birks HH. Full-glacial upland tundra vegetation preserved under tephra in the Beringian National Park, Seward Peninsula, Alaska. Quat Sci Rev. 2001;20:135–147.

Alsos IG, Engelskjøn T, Gielly L, Taberlet P, Brochmann C. Impact of ice ages on circumpolar molecular diversity: insights from an ecological key species. Mol Ecol. 2005;14:2739–2753. 10.1111/j.1365-294X.2005.02621.x PubMed DOI

Eidesen PB, Alsos IG, Popp M, Stensrud O, Suda J, Brochmann C. Nuclear vs. plastid data: complex Pleistocene history of a circumpolar key species. Mol Ecol. 2007;16:3902–3925. 10.1111/j.1365-294X.2007.03425.x PubMed DOI

Mardulyn P, Mikhailov Y, Pasteels JM. Testing phylogeographic hypotheses in a Euro-Siberian cold-adapted leaf beetle with coalescent simulations. Evolution. 2009;63:2717–2729. 10.1111/j.1558-5646.2009.00755.x PubMed DOI

Nève G, Barascud B, Descimon H, Baguette M. Gene flow rise with habitat fragmentation in the bog fritillary butterfly (Lepidoptera: Nymphalidae). BMC Evol Biol. 2008;8:84 10.1186/1471-2148-8-84 PubMed DOI PMC

Nève G, Pavlíčko A, Konvička M. Loss of genetic diversity through spontaneous colonization in the bog fritillary butterfly,

Tuzov VK, Bozano GC. Guide to the butterflies of the Palearctic region Nymphalidae, Part II, Tribe Argynnini:

Petersen B. Some trends of speciation in the cold-adapted Holarctic fauna. Zoologiska Bidrag från Uppsala. 1956;30:233–314.

Jakšić P, Van Swaay C, Đurić M.

Kudrna O, Pennerstorfer J, Lux K. Distribution atlas of European butterflies and skippers 3

Schtickzelle N, Turlure C, Baguette M. Grazing management impacts on the viability of the threatened bog fritillary butterfly

Klimczuk P, Sielezniew M. Unexpected differences in butterfly diversity between two peat bogs in the same area. Pol J Entomol. 2017; 86:251–273.

Tolman T, Lewington R. Collins butterfly guide: the most complete field guide to the butterflies of Britain and Europe. 3

Chernov YuI, Tatarinov AG. Butterflies (Lepidoptera, Rhopalocera) in the Arctic fauna. Entomol Rev. 2006;86(7):760–786.

Beneš J, Konvika M, Dvořák J, Fric Z, Havelda Z, Pavlíčko A, et al. Butterflies of the Czech Republic: Distribution and Conservation I, II. Prague: SOM; 2002.

Layberry RA, Hall PW, Lafontaine J. The Butterflies of Canada. Toronto: University of Toronto Press; 1998.

Tshikolovets VV. Butterflies of Europe & the Mediterranean area. Kiev: Tshikolovets; 2011.

Wahlberg N, Wheat CW. Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Syst Biol. 2008;57:231–242. 10.1080/10635150802033006 PubMed DOI

Monteiro A, Pierce NE. Phylogeny of PubMed DOI

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC

Clement M, Posada D, Crandall K. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–1660. PubMed

Leigh JW, Bryant D. PopART: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–1116.

Dellicour S, Mardulyn P. SPADS 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol Ecol Resour. 2014;14:647–651. 10.1111/1755-0998.12200 PubMed DOI

Excoffier L, Laval G, Schneider S. Arlequin vers. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online. 2005;1:47–50. PubMed PMC

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

Lanfear R, Calcott B, Ho Sy, Guindon S. Partition-finder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol, 2012;29:1695–1701. 10.1093/molbev/mss020 PubMed DOI

Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–1973. 10.1093/molbev/mss075 PubMed DOI PMC

Wahlberg N. That awkward age for butterflies: insights from the age of the butterfly subfamily Nymphalinae. Syst Biol. 2006;55:703–714. 10.1080/10635150600913235 PubMed DOI

Wahlberg N, Wheat CW, Peña C. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS One. 2013; 8(11):80875. PubMed PMC

Simonsen TJ, Wahlberg N, Warren AD, Sperling FAH. The evolutionary history of

Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214 10.1186/1471-2148-7-214 PubMed DOI PMC

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans: IEEE; 2010.

Tshikolovets VV, Bidzilya VO, Golovushkin MI. The butterflies of Transbaikal Siberia. Kiev, Pardubice: Tshikolovets; 2002.

Tshikolovets VV, Yakovlev RV, Bálint Z. The butterflies of Mongolia. Kiev, Pardubice: Tshikolovets; 2009.

Tshikolovets VV, Yakovlev RV, Kosterin OE. The butterflies of Altai, Sayans and Tuva (S.-W. Siberia). Kiev, Pardubice: Tshikolovets; 2009.

Tshikolovets VV, Nekrutenko YP. The butterflies of Caucasus and Transcaucasia (Armenia, Azerbaijan, Georgia and Russia). Kiev, Pardubice: Tshikolovets; 2012.

Tshikolovets VV, Kosterin O, Gorbunov P, Yakovlev R. The Butterflies of Kazakhstan. Kiev, Pardubice: Tshikolovets; 2016.

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965–1978.

Phillips SJ, Dudík M, Schapire RE. [Internet] Maxent software for modeling species niches and distributions (Version 3.4.1). [cited 2018 Nov 29]. http://biodiversityinformatics.amnh.org/open_source/maxent/.

Hijmans RJ, Phillips S, Leathwick J, Elith J. dismo: Species Distribution Modeling. R package version 1.1–4. 2017. https://cran.r-project.org/web/packages/dismo/dismo.pdf

Hijmans RJ. raster: Geographic Data Analysis and Modeling. R package version 2.8–4. 2018. https://cran.r-project.org/web/packages/raster/raster.pdf

Fourcade Y, Engler JO, Rodder D, Secondi J. Mapping species distributions with MAXENT using a geographically biased sample of presence data: A performance assessment of methods for correcting sampling bias. PLoS One. 2014;9:e97122 10.1371/journal.pone.0097122 PubMed DOI PMC

QGIS Development Team. [Internet] QGIS Geographic information system. Open source geospatial foundation project. [cited 2018 Nov 29]. http://qgis.osgeo.org.

Muscarella R, Galante PJ, Soley-Guardia M, Boria RA, Kass JM, Uriarte M, et al. ENMeval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for maxent eco- logical niche models. Methods Ecol Evol. 2014;5:1198–1205.

Fu Y-X. Statistical tests of neutrality of mutations against population growth, hitch- hiking, and background selection. Genetics. 1997;147:915–925. PubMed PMC

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–595. PubMed PMC

Ehlers J, Gibbard PL, Hughes PD. Quaternary glaciations—extent and chronology. Amsterdam: Elsevier; 2011.

Todisco V, Gratton P, Cesaroni D, Sbordoni V. Phylogeography of

Kleckova I, Cesanek M, Fric Z, Pellissier L. Diversification of the cold-adapted butterfly genus PubMed DOI

Peña C, Witthauer H, Klečková I, Fric Z, Wahlberg N. Adaptive radiations in butterflies: evolutionary history of the genus

Kodandaramaiah U, Wahlberg N. Phylogeny and biogeography of

Kodandaramaiah U, Braby MF, Grund R, Müller CJ, Wahlberg N. Phylogenetic relationships, biogeography and diversification of Coenonymphina butterflies (Nymphalidae: Satyrinae): intercontinental dispersal of a southern Gondwanan group?. Syst Entomol. 2018;43:798–809.

Varga Z. Das Prinzip der areal-analytischen Methode in der Zoogeographie und die Faunenelemente-Einteilung der europaäischen Tagschmetterlinge (Lepidoptera: Diurna). Acta Biologica Debrecina. 1977;14:223–285.

Sanmartin I, Enghoff H, Ronquist F. Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biol J Linn Soc Lond. 2001;73:345–390.

Mullen SP. Wing pattern evolution and the origins of mimicry among North American admiral butterflies (Nymphalidae: Limenitis). Mol Phylogenet Evol. 2006;39:747–758. 10.1016/j.ympev.2006.01.021 PubMed DOI

Kodandaramaiah U, Wahlberg N. Out-of-Africa origin and dispersal-mediated diversification of the butterfly genus PubMed DOI

Peña C, Nylin S, Freitas AVL, Wahlberg N. Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae). Zool Scr. 2010;39:243–258.

Peña C, Nylin S, Wahlberg N. The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Zool J Linn Soc. 2011;161:64–87.

Lafontaine JD, Wood DM. A zoogeographic analysis of the Noctuidae (Lepidoptera) of Beringia, and some inferences about past Beringian habitat. Memoirs of the Entomological Society of Canada. 1988;144:109–123.

Galbreath KE, Cook JA. Genetic consequences of Pleistocene glaciations for the tundra vole (Microtus oeconomus) in Beringia. Mol Ecol. 2004;13:135–148. PubMed

Hope AG, Takebayashi N, Galbreath KE, Talbot SL, Cook JA, Riddle B. Temporal, spatial and ecological dynamics of speciation among amphi‐Beringian small mammals. J Biogeogr. 2013;40:415–429.

Kohli BA, Fedorov VB, Waltari E, Cook JA. Phylogeography of a Holarctic rodent (

Dyke AS. (2004) An outline of North American Deglaciation with emphasis on central and northern Canada In: Ehlers J, Gibbard PL, editors. Quaternary Glaciations—Extent and Chronology, Part II. Amsterdam: Elsevier; 2004. p. 373–424.

Beatty GE, Provan JIM. Refugial persistence and postglacial recolonization of North America by the cold-tolerant herbaceous plant PubMed DOI

Godbout J, Jaramillo-Correa JP, Beaulieu J, Bosquet J. A mitochondrial DNA minisatellite reveals the postglacial history of jack pine ( PubMed DOI

Jackson ST, Webb RS, Anderson KH, Overpeck JT, Webb T III, Williams JW, et al. Vegetation and environment in Eastern North America during the Last Glacial Maximum. Quat Sci Rev. 2000;19:489–508.

Jaramillo‐Correa JP, Beaulieu J, Bousquet J. Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce ( PubMed DOI

Latutrie M, Bergeron Y, Tremblay F. Fine-scale assessment of genetic diversity of trembling aspen in northwestern North America. BMC Evol Biol. 2016;16:231 10.1186/s12862-016-0810-1 PubMed DOI PMC

Lee-Yaw JA, Irwin JT, Green DM. Postglacial range expansion from northern refugia by the wood frog, PubMed DOI

Li P, Li M, Shi Y, Zhao Y, Wan Y, Fu C, et al. Phylogeography of North American herbaceous PubMed DOI

Rowe KC, Heske EJ, Brown PW, Paige KN. Surviving the ice: Northern refugia and postglacial recolonization. Proc Natl Acad Sci U S A. 2004;101:10355–10359. 10.1073/pnas.0401338101 PubMed DOI PMC

Lait LA, Hebert P. Phylogeographic structure in three North American tent caterpillar species (Lepidoptera: Lasiocampidae): PubMed DOI PMC

Yakovlev RV, Shapoval NA, Kuftina GN, Kulak AV, Kovalev SV. Notes on the molecular taxonomy of the

Forister ML, Fordyce JA, Shapiro AM. Geological barriers and restricted gene flow in the holarctic skipper PubMed DOI

Gratton P, Konopinski MK, Sbordoni V. Pleistocene evolutionary history of the Clouded Apollo ( PubMed DOI

Wahlberg N, Saccheri I. The effects of Pleistocene glaciations on the phylogeography of

Bartonova A, Konvicka M, Korb S, Kramp K, Schmitt T, Faltynek Fric Z. (2018) Range dynamics of Palaearctic steppe species under glacial cycles: the phylogeography of

Svendsen JI, Alexanderson H, Astakhov VI, Demidov I, Dowdeswell JA, Funder S, et al. Late Quaternary ice sheet history of Eurasia. Quat Sci Rev. 2004;23:1229–1271.

Mägdefrau K. Paläobiologie der Pflanzen. Jena: Verlag Gustav Fischer; 1953.

Brunhoff C, Yoccoz NG, Ims RA, Jaarola M. Glacial survival or late glacial colonization? Phylogeography of the root vole (

Mikkola K, Lafontaine JD, Kononenko VS. Zoogeography of the Holarctic species of the Noctuidae (Lepidoptera): importance of the Beringian refuge. Entomol Fenn. 1991;2:157–173.

Quinzin MC, Normand S, Dellicour S, Svenning J-C, Mardulyn P. Glacial survival of trophically linked boreal species in northern Europe. Proc R Soc Lond B Biol Sci. 2017;284:20162799. PubMed PMC

Krzywicki M. Fauna Papilionoidea i Hesperioidea (Lepidoptera) Puszczy Białowieskiej. Annales Zoologici, Polska Akademia Nauk. 1967;25:1–213.

Sielezniew M, Ponikwicka-Tyszko D, Ratkiewicz M, Dziekanska I, Kostro-Amnroziak A, Rutkowski R. Divergent patterns in the mitochondrial and nuclear diversity of the specialized butterfly

Ratkiewicz M, Jaroszewicz B. Allopatric origins of sympatric forms: the skippers

Sielezniew M, Kostro-Ambroziak A, Klimczuk P, Deoniziak K, Pałka K, Nowicki P. Habitat-related differences in the adult longevity of two ecotypes of a specialized butterfly. J Zool. 2018;1–12.

Ehlers J, Astakhov V, Gibbard PL, Mangerud J, Svendsen JI. Middle Pleistocene in Eurasia In: Elias S, Mock C, editors. Encyclopedia of Quaternary Science. 2

Schmitt T. Biogeographical and evolutionary importance of the European high mountain systems. Front Zool. 2009;6:9 10.1186/1742-9994-6-9 PubMed DOI PMC

Nève G, Barascud B, Windig JJ. Population biology of

Dincă V, Runquist M, Nilsson M, Vila R. Dispersal, fragmentation, and isolation shape the phylogeography of the European lineages of

Horreo JL, Pelaez ML, Suárez T, Breedveld MC, Benoit H, Yann S-G, et al. Phylogeography, evolutionary history and effects of glaciations in a species (

Trettin J, Agrawal S, Heinze J. Phylogeography of social polymorphism in a boreo-montane ant. BMC Evol Biol. 2016;16:137 10.1186/s12862-016-0711-3 PubMed DOI PMC

Vences M, Hauswaldt JS, Steinfartz S, Rupp O, Goesmann A, Künzel S, et al. Radically different phylogeographies and patterns of genetic variation in two European brown frogs, genus PubMed DOI

Todisco V, Gratton P, Zakharov EV, Wheat CW, Sbordoni V, Sperling FAH. Mitochondrial phylogeography of the Holarctic

Hegna RH, Galarza JA, Mappes J. Global phylogeography and geographical variation in warning coloration of the wood tiger moth (

Kodandaramaiah U, Weingartner E, Janz N, Dalén L, Nylin S. Population structure in relation to host-plant ecology and PubMed DOI

Kodandaramaiah U, Konvicka M, Tammaru T, Wahlberg N, Gotthard K. Phylogeography of the threatened butterfly, the woodland brown

Vandewoestijne S, Baguette M, Brakefield PM, Saccheri IJ. Phylogeography of PubMed DOI

Konvicka M, Zimmermann K, Klimova M, Hula V, Fric Z. Inverse link between density and dispersal distance in butterflies: field evidence from six co-occurring species. Popul Ecol. 2012;54:91–101.

Mennechez G, Schtickzelle N, Baguette M. Metapopulation dynamics of the bog fritillary butterfly: comparison of demographic parameters and dispersal between a continuous and a highly fragmented landscape. Lands Ecol. 2003;18:279–291.

Habel JC, Schmitt T. The burden of genetic diversity. Biol Conserv. 2012;147:270–274.

Eastern Arc of Glacial Relict Species-Population Genetics of Violet Copper Lycaena helle Butterfly in East-Central Europe

A haplotype-resolved, de novo genome assembly for the wood tiger moth (Arctia plantaginis) through trio binning