- Open Access
Extra-Mediterranean refugia: The rule and not the exception?
© Schmitt and Varga; licensee BioMed Central Ltd. 2012
- Received: 29 June 2012
- Accepted: 28 August 2012
- Published: 6 September 2012
Some decades ago, biogeographers distinguished three major faunal types of high importance for Europe: (i) Mediterranean elements with exclusive glacial survival in the Mediterranean refugia, (ii) Siberian elements with glacial refugia in the eastern Palearctic and only postglacial expansion to Europe and (iii) arctic and/or alpine elements with large zonal distributions in the periglacial areas and postglacial retreat to the North and/or into the high mountain systems. Genetic analyses have unravelled numerous additional refugia both of continental and Mediterranean species, thus strongly modifying the biogeographical view of Europe. This modified notion is particularly true for the so-called Siberian species, which in many cases have not immigrated into Europe during the postglacial period, but most likely have survived the last, or even several glacial phases, in extra-Mediterranean refugia in some climatically favourable but geographically limited areas of southern Central and Eastern Europe. Recently, genetic analyses revealed that typical Mediterranean species have also survived the Last Glacial Maximum in cryptic northern refugia (e.g. in the Carpathians or even north of the Alps) in addition to their Mediterranean refuge areas.
- Faunal types
- Last Glacial Maximum (LGM)
- Range expansions
- Range shifts
The biogeography of the western Palearctic is quite complex and therefore a fascinating and challenging research subject [1–8]. Scientists, even about 50 years ago, distinguished three major faunal components in Europe (Mediterranean, Siberian, arctic and/or alpine), but the interpretation of the underlying biogeographical processes behind these faunal elements has considerably changed since then, e.g. [8–13]. Furthermore, the understanding of climatic and other environmental conditions during glaciations has substantially deepened, e.g. [14–19].
Furthermore, the existence of large ice age distributions in the zonal periglacial belt was suggested for the species with arctic, alpine or arctic-alpine distributions followed by postglacial retreat to high mountain areas in the South and/or the high latitudes in the North. Retreat into both directions was interpreted as the reason for the arctic-alpine disjunctions today [22, 23]. However, local endemics e.g. in the Alps were interpreted (at least partly) as in situ survival e.g. at nunataks  and/or in some marginal areas of the Alps (“massifs de refuge”, ) and other southern European high mountain systems [25, 26]. Thus, the more widespread species in this group were interpreted, following the old monoglacial ideas of Scharff , as the only species surviving north of the mountain chains of the Pyrenees, Alps and Carpathians (Figure 1b).
Over the past two decades genetic analyses of many animal and plant species, representing different biogeographical groups, have strongly enhanced our understanding of the highly complex biogeographical patterns and processes within the western Palearctic [5–8, 10, 40–44]. Therefore, we review the changing view with respect to extra-Mediterranean refugia with a special focus on the geographic location of these refugia, their mostly limited spatial extent and often cryptic natures. As recent reviews already address these extra-Mediterranean refugia in artic/alpine species [10, 45–48], we focus in this article on continental and Mediterranean species.
The species with typical continental distribution patterns (i.e. not reaching the areas with typical Atlantic and Mediterranean climates, but being widely distributed from continental Europe throughout temperate Asia) were formerly thought to have immigrated to Europe from eastern Asiatic Würm glacial refuge areas (i.e. from the Siberian and the Manchurian core areas) during the postglacial period (Figure 1c) . However, this idea was questioned afterwards on the basis of chorological (i.e. the classical interpretation of distribution patterns) and intraspecific taxonomical analyses (cf. Figure 2). Consequently, survival of such continental species was postulated in Europe outside the classical Mediterranean refuge areas [25, 29–33].
A complex hierarchical pattern was also observed in the adder Vipera berus, a snake distributed from western Europe throughout Asia as far east as the island of Sakhalin. Ursenbacher et al.  showed a strong differentiation into three major genetic lineages of most probably pre-Pleistocene origin with two of these being geographically restricted (northern Italian Alps; western Balkan mountains) and one being fairly widespread from France and the UK to the Pacific. The widespread lineage is further divided into several sub-clades of which all apart from one are confined to some part of Europe. These data suggest that two relict lineages most probably survived long periods of time (maybe even the whole Pleistocene) in extra-Mediterranean regions at the southern Alps margin and in the mountainous regions of the western Balkan Peninsula.
The sibling Vipera seoanei, restricted to the mountain ranges of northern Iberia, is even more strongly differentiated from V. berus than the lineages within this latter species . The split between these two species probably occurred before the beginning of the glacial-interglacial cycles, with V. seoanei most likely having continuously existed over time in the extra-Mediterranean regions of Iberia. It is in this area that the species has two morphologically differentiated subspecies , thus indicating two centres of glacial survival.
Furthermore, mtDNA analyses of the snail Arion fuscus support an extra-Mediterranean survival of this species especially in the eastern regions of the Alps, but maybe also in other extra-Mediterranean retreats such as in the area of the Tatras . A strongly differentiated lineage of this species is restricted to the Balkan Peninsula. Whether the respective refugia have to be considered Ponto-Mediterranean or Balkan extra-Mediterranean is in need of further genetic analyses.
Surveys of the bank vole (Clethrionomys glareolus) have not only shown the significance of “northern” refugia in the Carpathians, but also in some other areas, e.g., the vicinity of the Alps, southern France, and southern parts of the Ural Mountains (Figure 6b). New fossil and genetic records support the refugial character of the southern Urals in eastern Europe. Recently, a morphometric analysis of bank vole molars has unravelled the existence of a “Ural” morphotype of this species .
Although the transitional forest steppic character of the LGM vegetation of the Russian plain already was demonstrated in several palaeo-ecological publications e.g. [76, 77], the importance of the refugia in the Urals (Figure 6), also in Kazakhstan and south-western Siberia was only recently shown [67, 78, 79], and Danukalova et al.  pointed out that “the changes of the palaeoenvironment were not so sharp as in the adjacent northwestern territories. Biota of the region has been formed under the influence of the European and Asiatic elements”.
For common shrews (Sorex araneus), two major continental refugia have been discovered, one in the southern Urals, from which the re-population of northern Europe started, and a southern Siberian core area which shows a geographic co-incidence with some nemoral species (; further details e.g. in Walter and Straka ; Walter and Breckle ). These results have been repeatedly confirmed by the karyological and molecular analyses of Wóycik et al. , and also perfectly harmonise with the suggested history of postglacial expansion of C. glareolus from a southern continental core area (Urals) to northern Russia . Additionally, in forest bird species, the Caucasus appears to be an area of genetic divergence. Endemic (or nearly so) clusters of haplotypes in the Caucasus have been documented for several species (Carpodacus erythrinus, Motacilla alba Sitta europaea Troglodytes troglodytes; reviewed by Zink et al. ).
All these examples clearly show that the continental species have had much more refugia and thus, performed much smaller range shifts and expansions than previously thought. Expansion from Siberian core areas into Europe have only been demonstrated in mobile species of boreo-temperate forests such as the great spotted woodpecker (Dendrocopus maior), the boreal warbler (Phylloscopus borealis), the Siberian flying squirrel (Pteromys volans), or the wood lemming (Myopus schisticolor) [84–87]. These species exhibit a higher level of genetic differentiation only at the eastern-southeastern parts of their distributions. Additionally, the dwarf damselfly Nehalennia speciosa, a specialist species of oligotrophic peat bogs, shows a very shallow differentiation all over the Palearctic and most probably expanded from an eastern Asiatic ice age refuge at the beginning of the postglacial period . Some species of boreal forests have had at least two subsequent waves of expansion from the eastern Palaearctic to Europe, from which the representatives of the earlier ones have been preserved in some southern European high mountains as the Pyrenees, the Cantabrian mountains and/or in the Balkans, as e.g. the capercaille [89, 90].
For Holarctic boreal forest species, a deeper split has only been shown between the Nearctic and the Palearctic populations (e.g. the birds Picoides tridactylus, Pinicola enucleator, Troglodytes troglodytes), mostly connected with stronger genetic differentiation in the Nearctic [84, 91, 92]. Therefore, a direct Siberian invasion to Europe is rare and can only be supported for some boreal forest species by shallow phylogeographic structures. This pattern might be the strict exception in temperate non-forest species and not one of the paradigms as postulated by de Lattin .
In general, these extra-Mediterranean refugia were apparently often located in the vicinity of water donating mountains systems as the glaciated Alps, Carpathians or Balkan mountain systems cf. , which may have received more precipitation during the kryoxerotic LGM than the adjacent lowland loess steppe areas. The same idea implicitly appears in some recent papers of Bhagwat and Willis , Varga  and Stewart et al. supported by habitat preference data of numerous, mostly woody plant and vertebrate species. Furthermore, many of these refugia must have been small and sporadic in their geographic extent [93, 94] so that they have been overlooked in the past reconstruction of the glacial faunas mostly based on fossil records. This might explain their cryptic character, which is in clear contrast to their great importance for the re-colonisation of major parts of Europe, a fact that could only be demonstrated by the recent genetic analyses.
De Lattin’s paradigm  of survival of thermophilic animal and plant species exclusively in Mediterranean Würm refugia remained untouched until quite recently. However, evidence has accumulated that glacial distribution patterns were considerably more intricate than previously thought [8, 38], and even additional extra-Mediterranean ice age refugia are looking more and more likely for some of these Mediterranean taxa [11, 12]. The combination of southern and continental refugia became especially evident in the often cited case of the “paradigmatic” brown bear, e.g. [42, 62, 74, 95]. The successful extraction and sequencing of mtDNA from fossil bones has shown the highly complex phylogeographic pattern of this species [68, 69, 71–73]. Thus, the predictions of the “expansion-contraction” (E/C) model were not supported, and consequently the classic glacial refugium model is insufficient to explain the genetic history of European brown bears.
Furthermore, Fink et al.  found a genetic lineage in the rodent Microtus arvalis, endemic to the region of the Black Forest (south-western Germany). Tougard et al.  described two more lineages of this species, which most likely have evolved in extra-Mediterranean refugia of Central and East Europe, including the Carpathian Basin. Consequently, M. arvalis survived at least the last ice age in a complex system of extra-Mediterranean and classical Mediterranean core areas. However, we have to assume that the more northern part of the glacial distribution of this vole was, at least transitionally, restricted to geographically small regions with a more buffered climate, thus only some extra-zonal areas in the periglacial tundra and steppe region, although M. arvalis in general was a common component of fossil remains of last glacial faunas .
A large number of recent publications have shown the great importance of extra-Mediterranean refugia for temperate species and not only for alpine and arctic taxa. While the latter two groups may have frequently had wide ranges over this cold-continental zonobiome , the glacial range contractions of thermophilic temperate species, in most cases, must have led to small (and very small) meso- or microclimatically favourable extra- or intrazonal areas within the extended periglacial belt.
Many species with typical continental distributions might have had glacial distribution patterns with multiple extra-Mediterranean refugia, and were mostly not restricted to refuge areas in the eastern Palearctic, as often previously thought. However, this is not to say that they were absent from the eastern Palearctic, but these contractions were not the exclusive ones for these species.
Instead, recent research showed that even thermophilic species, which were formerly thought of having been completely restricted to Mediterranean core areas, could in some cases survive in extra-Mediterranean refugia in addition to the typical Mediterranean areas. Such populations in many cases have an even higher genetic diversity and expansive power than populations restricted to the more southern “classical” refugia.
These observations can be explained by two different factors, which might have acted in combination. The southern refugia of temperate species were often surrounded by extended cold-arid steppe areas, e.g. in the central part of the Balkan Peninsula and also in the Carpathian Basin . Furthermore, the populations of the scattered extra-Mediterranean refugial pockets could expand and hybridise among each other during the milder interstadial phases of the Würm and also between the LGM and the younger Dryas period . It means that these extra-Mediterranean refuge populations have survived at the rear edge of the range during the ice ages, with all evolutionary consequences of this situation . These ice age rear edges became the leading edges of the postglacial northwards range expansions, thus strongly impacting the genetic constitution of Central and North Europe in many plant and animal species. In many cases, such populations have been characterised as localised subspecies of extended polytypic continental species, and they are considered as evolutionarily significant units (ESUs) of high conservation priority .
For all these reasons, the extra-Mediterranean refugia apparently represent an important biogeographical component of the western Palaearctic, maybe nearly equivalent to the Mediterranean refugia further south.
Through these new findings, we can also answer the question of the article’s title: whether extra-Mediterranean refugia are the rule or the exception. In fact, they are a bit of both. Extra-Mediterranean refugia have been a common feature during, at least, the last ice age and thus are paradigmatic. However, they are also represented by many individual patterns of particular biogeographical features so that each case shows at least some uniqueness. The principle of individual responses of the species to climatic oscillations between glacial and interglacial conditions was repeatedly postulated in this context (cf. Stewart et al., , but also see Bhagwat & Willis ). During glaciations, ecosystems that exist today had been largely disintegrated and were represented by de novo ecosystems without close connection with the succeeding ones (e.g. the mammoth steppe with tundra, cold steppic and alpine elements). These ecosystems were locally intermingled with small forest refugia (i.e. the pockets of forests of Bhagwat & Willis, ) and also showed non-analogous mammal assemblages [13, 35, 77, 115].
Therefore, no regular North–South shifts took place between glacial and interglacial conditions and vice versa (as implicitly assumed in the biogeographical range paradigms, cf. [5, 6]). Instead, a new sequence of ecosystems always had to be established, influenced by a combination of precipitation and temperature. The newly evolved macro-biome of a continental cold steppe (that no longer exists) must have had characteristic macro-ecotones against the (glacially reduced) boreal forests and against the continental meadow steppes of temperate latitudes.
Although not existing under the recent climatic conditions, these macro-ecotones can be modelled based on the zonality of the cold-continental conditions of southern Siberia, northern Mongolia or even Yakutia. Here, many floral and faunal elements can be observed together on species-rich meadow steppes of these regions, species assemblages, which are partitioned to different habitats in eastern Europe like dry steppic grasslands, meadow steppes, damp meadows or even salt meadows. The large number of macro-ecotones with their specific species assemblages is the background for the phenomenon of the evolution of so many species specific biogeographies, but hereby also for the paradigmatic patterns, i.e. the regular existence of micro-refugia. However, this is only a special case of the law of uniformity because even today such micro-refugia with peculiar mixtures of faunal and floral elements exist under analogous climatic conditions.
Both authors wrote this article in equal parts. Both authors read and approved the final manuscript.
Thomas Schmitt is Professor of Molecular Biogeography at Trier University. His main scientific interests are biogeography (classical and molecular), ecology (classical and molecular), evolutionary biology, conservation biology as well as the taxonomy of butterflies. He also has a special interest in the high mountain systems of the western Palearctic.
Zoltán Varga is Professor emeritus of Zoology at the University of Debrecen. His scientific focus is on biogeography, evolutionary biology, conservation biology and ecology as well as the taxonomy of butterflies and noctuid moths. He is one of the leading experts for the Carpathian Basin, the Balkan Peninsula and the arid zones of Central Asia.
- Reinig W: Die Holarktis. 1937, Fischer, JenaGoogle Scholar
- Reinig W: Chorologische Voraussetzungen für die Analyse von Formenkreisen. Syllegomena biologica: Festschrift zum 80. Geburtstage von Otto Kleinschmidt. Edited by: Jordans A, Peus F, Kleinschmidt O. 1950, Ziemsen, Leipzig, 346-378.Google Scholar
- De Lattin G: Die Ausbreitungszentren der holarktischen Landtierwelt. Verhandlungen der Deutschen Zoologischen Gesellschaft vom 21. bis 26. Mai 1956 in Hamburg. Edited by: Pflugfelder O. 1957, Geest & Portig, Leipzig, 380-410.Google Scholar
- De Lattin G: Grundriß der Zoogeographie. 1967, Verlag Gustav Fischer, JenaGoogle Scholar
- Hewitt GM: Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc. 1996, 58: 247-276.Google Scholar
- Hewitt GM: Post-glacial re-colonization of European biota. Biol J Linn Soc. 1999, 68: 87-112. 10.1111/j.1095-8312.1999.tb01160.x.Google Scholar
- Hewitt GM: The genetic legacy of the Quaternary ice ages. Nature. 2000, 405: 907-913. 10.1038/35016000.PubMedGoogle Scholar
- Schmitt T: Molecular Biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool. 2007, 4: 11-10.1186/1742-9994-4-11.PubMed CentralPubMedGoogle Scholar
- Stewart JR, Lister AM: Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol. 2001, 16: 608-613. 10.1016/S0169-5347(01)02338-2.Google Scholar
- Schmitt T: Biogeographical and evolutionary importance of the European high mountain systems. Front Zool. 2009, 6: 9-10.1186/1742-9994-6-9.PubMed CentralPubMedGoogle Scholar
- Provan J, Bennett KD: Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol. 2008, 23: 564-571. 10.1016/j.tree.2008.06.010.PubMedGoogle Scholar
- Stewart JR, Lister AM, Barnes I, Dalén L: Refugia revisited: individualistic responses of species in space and time. Proc R Soc B. 2010, 277: 661-671. 10.1098/rspb.2009.1272.PubMed CentralPubMedGoogle Scholar
- Varga Z: Extra-Mediterranean refugia, post-glacial vegetation history and area dynamics in Eastern Central Europe. Relict Species: Phylogeography and Conservation Biology. Edited by: Habel JC, Assmann T. 2010, Springer, Heidelberg, 57-87.Google Scholar
- Huybers P, Wunsch C: Obliquity pacing of the late Pleistocene glacial terminations. Nature. 2005, 434: 491-494. 10.1038/nature03401.PubMedGoogle Scholar
- Jahn A, Claussen M, Ganopolski A, Brovkin V: Quantifying the effect of vegetation dynamics on the climate of the Last Glacial Maximum. Clim Past Discuss. 2005, 1: 1-16. 10.5194/cpd-1-1-2005.Google Scholar
- Quante M: The Changing Climate: Past, Present, Future. Relict Species: Phylogeography and Conservation Biology. Edited by: Habel JC, Assmann T. 2010, Springer, Heidelberg, 9-56.Google Scholar
- Willis KJ, Bhagwat SA: Questions of importance to the conservation of biological diversity: answers from the past. Clim Past Discuss. 2010, 6: 759-769.Google Scholar
- De Bruyn M, Hoelzel R, Carvalho GR, Hofreiter M: Faunal histories from Holocene ancient DNA. Trends Ecol Evol. 2011, 26: 405-413. 10.1016/j.tree.2011.03.021.PubMedGoogle Scholar
- Woillez M-N, Kageyama M, Krinner G, de Noblet-Ducoudré N, Viovy N, Mancip M: Impact of CO2 and climate on the Last Glacial Maximum vegetation: results from the ORCHIDEE/IPSL models. Clim Past. 2011, 7: 557-577. 10.5194/cp-7-557-2011.Google Scholar
- Rebel H: Zur Frage der europäischen Faunenelemente. Annalen Naturhist Mus Wien. 1931, 46: 49-55.Google Scholar
- De Lattin G: Beiträge zur Zoogeographie des Mittelmeergebietes. Verh Dt Zool Ges. 1949, 42: 143-151.Google Scholar
- Holdhaus K, Lindroth C: Die europäischen Koleopteren mit boreo-alpiner Verbreitung. Annalen Naturhist Mus Wien. 1939, 50: 123-293.Google Scholar
- Holdhaus K: Die Spuren der Eiszeit in der Tierwelt Europas. 1954, Universitätsverlag Wagener, InnsbruckGoogle Scholar
- Jeannel R: La genèse des faunes terrestres. 1943, Presses Universitaires de France, ParisGoogle Scholar
- Varga Z: Geographische Isolation und Subspeziation bei den Hochgebirgs-Lepidopteren der Balkanhalbinsel. Acta Entomol Jugoslavica. 1975, 11: 5-40.Google Scholar
- Varga Z: Biogeography and Evolution of the oreal Lepidoptera in the Palearctic. Acta Zool Hung. 1996, 42: 289-330.Google Scholar
- Scharff RF: The history of the European fauna. 1899, Walter Scott, LondonGoogle Scholar
- De Lattin G: Die Verbreitung des sibirischen Faunenelements in der Westpaläarktis. Nat Mus. 1964, 94: 104-125.Google Scholar
- Varga Z: Taxonomic survey of the SE-European forms of Melitaea phoebe Schiff. (Lep.: Nymphalidae) with description of two new subspecies (in Hungarian with English summary). Acta Biol Debrecina. 1967, 5: 119-137.Google Scholar
- Varga Z: Das Prinzip der areal-analytischen Methode in der Zoogeographie und die Faunenelemente-Einteilung der europäischen Tagschmetterlinge (Lep.: Diurna). Acta Biol Debrecina. 1977, 14: 223-285.Google Scholar
- Aspöck H, Aspöck U, Rausch H: Polyzentrische Ausbreitung eines "Sibirisch-mediterranen" Faunenelements am Beispiel der Polytypischen Kamelhalsfliege Raphidia ophiopsis L. (Neuroptera, Raphidioptera, Raphidiidae). Zeitschr Arbeitsgem Österr Entomol. 1976, 28: 89-105.Google Scholar
- Aspöck H: Die Herkunft der Raphidiopteren des extramediterranen Europa - eine kritische biogeographische Analyse. Verhandlungen des VII. 1979, Internationalen Symposiums über Entomofaunistik in Mitteleuropa, 1977, Leningrad, 14-22.Google Scholar
- Malicky H: Chorological patterns and biome types of European Trichoptera and other freshwater insects. Archiv Hydrobiol. 1983, 96: 223-244.Google Scholar
- Kotlík P, Deffontaine V, Mascheretti S, Zima J, Michaux JR, Searle JB: A northern glacial refugium for bank voles (Clethrionomys glareolus). Proc Natl Acad Sci USA. 2006, 103: 14860-14864. 10.1073/pnas.0603237103.PubMed CentralPubMedGoogle Scholar
- Sommer RS, Nadachowski A: Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Rev. 2006, 36: 251-265. 10.1111/j.1365-2907.2006.00093.x.Google Scholar
- Bhagwat SA, Willis KJ: Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits?. J Biogeogr. 2008, 35: 464-482. 10.1111/j.1365-2699.2007.01861.x.Google Scholar
- Birks HJB, Willis KJ: Alpines, trees, and refugia in Europe. Plant Ecol Divers. 2008, 1: 147-160. 10.1080/17550870802349146.Google Scholar
- Svenning J-C, Normand S, Kageyama M: Glacial refugia of temperate trees in Europe: insights from species distribution modelling. J Ecol. 2008, 96: 1117-1127. 10.1111/j.1365-2745.2008.01422.x.Google Scholar
- Varga Z: Extension, isolation, micro-évolution. Acta Biol Debrecina. 1971, 8: 195-211.Google Scholar
- Hewitt GM: Speciation, hybrid zones and phylogeography — or seeing genes in space and time. Mol Ecol. 2001, 10: 537-549.PubMedGoogle Scholar
- Hewitt GM: Genetic consequences of climatic oscillation in the Quaternary. Phil Trans R Soc Lond B. 2004, 359: 183-195. 10.1098/rstb.2003.1388.Google Scholar
- Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F: Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol. 1998, 7: 453-464. 10.1046/j.1365-294x.1998.00289.x.PubMedGoogle Scholar
- Habel JC, Schmitt T, Müller P: The fourth paradigm pattern of post-glacial range expansion of European terrestrial species: the phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera). J Biogeogr. 2005, 32: 1489-1497. 10.1111/j.1365-2699.2005.01273.x.Google Scholar
- Randi E: Phylogeography of South European mammals. Phylogeography of Southern European Refugia. Edited by: Weiss S, Ferrand N. 2007, Springer, Dordrecht, 101-126.Google Scholar
- Tribsch A, Schönswetter P: In search for Pleistocene refugia for mountain plants: patterns of endemism and comparative phylogeography confirm palaeo-environmental evidence in the Eastern European Alps. Taxon. 2003, 52: 477-497. 10.2307/3647447.Google Scholar
- Schönswetter P, Stehlik I, Holderegger R, Tribsch A: Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol. 2005, 14: 3547-3555. 10.1111/j.1365-294X.2005.02683.x.PubMedGoogle Scholar
- Holderegger R, Thiel-Egenter C: A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. J Biogeogr. 2009, 36: 476-480. 10.1111/j.1365-2699.2008.02027.x.Google Scholar
- Schmitt T, Muster C, Schönswetter P: Are disjunct alpine and arctic-alpine animal and plant species in the western Palearctic really "relics of a cold past"?. Relict Species: Phylogeography and Conservation Biology. Edited by: Habel JC, Assmann T. 2010, Springer, Heidelberg, 239-252.Google Scholar
- Schmitt T, Varga Z, Seitz A: Forests as dispersal barriers for Erebia medusa (Nymphalidae, Lepidoptera). Basic Appl Ecol. 2000, 1: 53-59. 10.1078/1439-1791-00008.Google Scholar
- Schmitt T, Rákosy L, Abadjiev S, Müller P: Multiple differentiation centres of a non-Mediterranean butterfly species in south-eastern Europe. J Biogeogr. 2007, 34: 939-950. 10.1111/j.1365-2699.2006.01684.x.Google Scholar
- Schmitt T, Seitz A: Intraspecific allozymatic differentiation reveals the glacial refugia and the postglacial expansions of European Erebia medusa (Lepidoptera: Nymphalidae). Biol J Linn Soc. 2001, 74: 429-458.Google Scholar
- Schmitt T, Müller P: Limited hybridization along a large contact zone between two genetic lineages of the butterfly Erebia medusa (Satyrinae, Lepidoptera) in Central Europe. J Zool Syst Evol Res. 2007, 45: 39-46. 10.1111/j.1439-0469.2006.00404.x.Google Scholar
- Hammouti N, Schmitt T, Seitz A, Kosuch J, Veith M: Combining mitochondrial and nuclear evidences: a refined evolutionary history of Erebia medusa (Lepidoptera: Nymphalidae: Satyrinae) in Central Europe based on the CO1 gene. J Zool Syst Evol Res. 2010, 48: 115-125. 10.1111/j.1439-0469.2009.00544.x.Google Scholar
- Gratton P, Konopinski MK, Sbordoni V: Pleistocene evolutionary history of the Clouded Apollo (Parnassius mnemosyne): genetic signatures of climate cycles and a 'time-dependent' mitochondrial substitution rate. Mol Ecol. 2008, 17: 4248-4262. 10.1111/j.1365-294X.2008.03901.x.PubMedGoogle Scholar
- Ursenbacher S, Carlsson M, Helfer V, Tegelström H, Fumagalli L: Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Mol Ecol. 2006, 15: 3425-3437. 10.1111/j.1365-294X.2006.03031.x.PubMedGoogle Scholar
- Martínez Freiría F: Biogeografía y ecología de las víboras ibéricas (Vipera aspis, V. latastei y V. seoanei) en una zona de contacto en el norte peninsular. PhD thesis. 2009, University of Salamanca,Google Scholar
- Pinceel J, Jordaens K, Pfenninger M, Backeljau T: Rangewide phylogeography of a terrestrial slug in Europe: evidence for Alpine refugia and rapid colonization after the Pleistocene glaciations. Mol Ecol. 2005, 14: 1133-1150. 10.1111/j.1365-294X.2005.02479.x.PubMedGoogle Scholar
- Jaarola M, Searle JB: Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol. 2002, 11: 2613-2621. 10.1046/j.1365-294X.2002.01639.x.PubMedGoogle Scholar
- Babik W, Branicki W, Sandera M, Litvinchuk S, Borkin LJ, Irwin JT, Rafinski J: Mitochondrial phylogeography of the moor frog, Rana arvalis. Mol Ecol. 2004, 13: 1469-1480. 10.1111/j.1365-294X.2004.02157.x.PubMedGoogle Scholar
- Deffontaine V, Libois R, Kotlík P, Sommer R, Nieberding C, Paradis E, Searle JB, Michaux JR: 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. 10.1111/j.1365-294X.2005.02506.x.PubMedGoogle Scholar
- Joger U, Fritz U, Guicking D, Kalyabina-Hauf S, Nagy ZT, Wink M: Phylogeography of western Palaearctic reptiles: Spatial and temporal speciation patterns. Zool Anz. 2007, 246: 293-313. 10.1016/j.jcz.2007.09.002.Google Scholar
- Saarma U, Ho SYW, Pybus OG, Kaljuste M, Tumanov IL, Kojola I, Vorobiev AA, Markov NI, Saveljev AP, Valdmann H, Lyapunova EA, Abramov AV, Männil P, Korsten M, Vulla E, Pazetnov SV, Pazetnov VS, Putchkovskiy SV, Rokov AM: Mitogenetic structure of brown bears (Ursus arctos L.) in north-eastern Europe and a new time frame for the formation of European brown bear lineages. Mol Ecol. 2007, 16: 401-413.PubMedGoogle Scholar
- Tougard C, Renvoisé E, Petitjean A, Quéré J-P: New insight into the colonization processes of common voles: inferences from molecular and fossil evidence. PLoS One. 2008, 3: e3532-10.1371/journal.pone.0003532.PubMed CentralPubMedGoogle Scholar
- Davison J, Ho SYW, Bray SC, Korsten M, Tammeleht E, Hindrikson M, Østbye K, Østbye E, Lauritzen S-E, Austin J, Cooper A, Saarma U: Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species. Quat Sci Rev. 2011, 30: 418-430. 10.1016/j.quascirev.2010.11.023.Google Scholar
- Kupriyanova LA, Mayer W, Böhme W: Karyotype diversity of the Eurasian lizard Zootoca vivipara (Jacquin, 1787) from Central Europe and the evolution of viviparity. Proceedings of the 13th Congress of the Societas Europaea Herpetologica. 2006, 67-72.Google Scholar
- Surget-Groba Y, Heulin B, Guillaume C-P, Puky M, Semenov B, Orlova V, Kupriyanova L, Ghira I, Smajda B: Multiple origins of viviparity, or reversal from viviparity to oviparity and the evolution of parity. Biol J Linn Soc. 2006, 87: 1-11. 10.1111/j.1095-8312.2006.00552.x.Google Scholar
- Polyakov AV, Panov VV, Ladygina TY, Bochkarev MN, Rodionova MI, Borodin PM: Chromosomal Evolution of the Common Shrew Sorex araneus L. from the Southern Urals and Siberia in the Postglacial Period. Russ J Genet. 2001, 37: 351-357. 10.1023/A:1016690023394.Google Scholar
- Hofreiter M, Serre D, Rohland N, Rabeder G, Nagel D, Conard N, Münzel S, Pääbo S: Lack of phylogeography in European mammals before the last glaciation. Proc Natl Acad USA. 2004, 101: 12963-12968. 10.1073/pnas.0403618101.Google Scholar
- Hedrick P, Waits L: What the ancient DNA tells us?. Heredity. 2005, 94: 463-464. 10.1038/sj.hdy.6800647.PubMedGoogle Scholar
- Neumann K, Michaux JR, Maak S, Jansman HAH, Kayser A, Mundt G, Gattermann R: Genetic spatial structure of European common hamsters (Cricetus cricetus) — a result of repeated range expansion and demographic bottlenecks. Mol Ecol. 2005, 14: 1473-1483. 10.1111/j.1365-294X.2005.02519.x.PubMedGoogle Scholar
- Valdiosera CE, Garcia N, Anderlung C, Dalen L, Cregut-Bonnoure E, Kahlke RD, Stiller M, Brandström M, Thomas MG, Arsuaga J-L, Götherström A, Barnes I: Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Mol Ecol. 2007, 16: 5140-5148. 10.1111/j.1365-294X.2007.03590.x.PubMedGoogle Scholar
- Ho SYW, Saarma U, Barnett R, Haile J, Shapiro B: The effect of inappropriate calibration: three case studies in molecular ecology. PLoS One. 2008, 3: e1615-10.1371/journal.pone.0001615.PubMed CentralPubMedGoogle Scholar
- Krause J, Unger T, Noçon A, Malaspinas A-S, Kolokotronis S-O, Stiller M, Soibelzon L, Spriggs H, Dear PH, Briggs A-W, Bray SCE, O'Brien SJ, Rabeder G, Matheus P, Cooper A, Slatkin M, Pääbo S, Hofreiter M: Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. BMC Evol Biol. 2008, 8: 220-10.1186/1471-2148-8-220.PubMed CentralPubMedGoogle Scholar
- Korsten M, Ho SYW, Davison J, Pähn B, Vulla E, Roht M, Tumanov IL, Kojola I, Andersone-Lilley Z, Ozolins J, Pilot M, Mertzanis Y, Giannakopoulos A, Vorobiev AA, Markov NI, Saveljev AP, Lyapunova EA, Abramov AV, Männil P, Valdmann H, Pazetnov SV, Pazetnov VS, Rokov AM, Saarma U: Sudden expansion of a single brown bear maternal lineage across northern continental Eurasia after the last ice age: a general demographic model for mammals?. Mol Ecol. 2009, 18: 1963-1979. 10.1111/j.1365-294X.2009.04163.x.PubMedGoogle Scholar
- Ledevin R, Michaux JR, Deffontaine V, Henttonen H, Renaud S: Evolutionary history of the bank vole Myodes glareolus: a morphometric perspective. Biol J Linn Soc. 2010, 100: 681-694. 10.1111/j.1095-8312.2010.01445.x.Google Scholar
- Velichko AA, Catto N, Drenova AN, Klimanova VA, Kremenetskia KV, Nechaeva VP: Climate changes in East Europe and Siberia at the Late glacial–holocene transition. Quat Internat. 2002, 91: 75-99. 10.1016/S1040-6182(01)00104-5.Google Scholar
- Simakova AN: The vegetation of the Russian Plain during the second part of the Late Pleistocene (33–18 ka). Quat Internat. 2006, 149: 110-114. 10.1016/j.quaint.2005.11.024.Google Scholar
- Danukalova G, Yakovlev A, Kosintcev P, Agadjanian A, Alimbekova L, Eremeev A, Morozova E: Quaternary fauna and flora of the Southern Urals region (Bashkortostan Republic). Quat Internat. 2009, 201: 13-24. 10.1016/j.quaint.2008.05.023.Google Scholar
- Horsák M, Chytry M, Danihelka J, Kocí M, Kubesova S, Kalososova Z, Otypkova Z, Tichy L: Snail faunas in the Ural forests and their relations to vegetation: an analogue of the early Holocene assemblages of Central Europe?. J Mollus Stud. 2010, 76: 1-10. 10.1093/mollus/eyp039.Google Scholar
- Walter H, Straka H: Arealkunde. Floristisch-historische Geobotanik. 1970, Ulmer, StuttgartGoogle Scholar
- Walter H, Breckle S-W: Ökologie der Erde. Spezielle Ökologie der Gemäßigten und Arktischen Zonen Euro-Nordasiens. 1986, Fischer, StuttgartGoogle Scholar
- Wójcik JM, Ratkiewicz M, Searle JB: Evolution of the common shrew Sorex araneus: chromosomal and molecular aspects. Acta Theriol. 2002, 47 (Suppl. 1): 139-167.Google Scholar
- Zink RM, Drovetski SV, Rohwer S: Selective neutrality of mitochondrial ND2 sequences, phylogeography and species limits in Sitta europaea. Mol Phylogen Evol. 2006, 40: 679-686. 10.1016/j.ympev.2005.11.002.Google Scholar
- Zink RM, Drovetski SV, Rohwer S: Phylogeographic patterns in the great spotted woodpecker Dendrocopos major across Eurasia. J Avian Biol. 2002, 33: 175-178. 10.1034/j.1600-048X.2002.330208.x.Google Scholar
- Oshida T, Abramov A, Yanagava H, Masuda R: Phylogeography of the Russian flying squirrel (Pteromys volans): implication of refugia theory in arboreal small mammal of Eurasia. Mol Ecol. 2005, 14: 1191-1196. 10.1111/j.1365-294X.2005.02475.x.PubMedGoogle Scholar
- Fedorov VB, Goropashnaya AV, Boeskorov GG, Fredga K: Comparative phylogeography and demographic history of the wood lemming (Myopus schisticolor): implications for late Quaternary history of the taiga species in Eurasia. Mol Ecol. 2008, 17: 598-610.PubMedGoogle Scholar
- Saitoh T, Alström P, Nishiumi I, Shigeta Y, Williams D, Olsson U, Ueda K: Old divergences in a boreal bird supports long-term survival through the ice ages. BMC Evol Biol. 2010, 10: 35-10.1186/1471-2148-10-35.PubMed CentralPubMedGoogle Scholar
- Bernard R, Heiser M, Hochkirch A, Schmitt T: Genetic homogeneity of the Sedgling Nehalennia speciosa (Odonata: Coenagrionidae) indicates a single Würm glacial refugium and trans-Palaearctic postglacial expansion. J Zool Syst Evol Res. 2011, 49: 292-297. 10.1111/j.1439-0469.2011.00630.x.Google Scholar
- Duriez O, Sachet JM, Menoni E, Miquel C, Taberlet P: Phylogeography of the capercaillie in Eurasia: what is the conservation status in the Pyrenees and Cantabrian mountains?. Conserv Genet. 2007, 8: 513-526. 10.1007/s10592-006-9165-2.Google Scholar
- Bajc M, Čas M, Ballian D, Kunovac S, Zubić G, Grubešić M, Zhelev P, Paule L, Kraigher H: Genetic differentiation of the western capercaillie highlights the importance of south-eastern Europe for understanding the species phylogeography. PLoS One. 2011, 6: e23602-10.1371/journal.pone.0023602.PubMed CentralPubMedGoogle Scholar
- Drovetski SV, Zink RM, Rohwer S, Fadeev IV, Nesterov EV, Karagodin I, Koblik EA, Redkin YA: Complex biogeographic history of a Holarctic passerine. Proc R Soc B. 2004, 271: 545-551. 10.1098/rspb.2003.2638.PubMed CentralPubMedGoogle Scholar
- Drovetski SV, Zink RM, Ericson PGP, Fadeev IV: A multilocus study of pine grosbeak phylogeography supports the pattern of greater intercontinental divergence in Holarctic boreal forest birds than in birds inhabiting other high-latitude habitats. J Biogeogr. 2010, 37: 696-706. 10.1111/j.1365-2699.2009.02234.x.Google Scholar
- Huck S, Büdel B, Kadereit JW, Printzen C: Range-wide phylogeography of the Europeam temperate montane herbaceous plant Meum athamanticum Jacq.: evidence for periglacial persistence. J Biogeogr. 2009, 36: 1588-1599. 10.1111/j.1365-2699.2009.02096.x.Google Scholar
- Huck S, Büdel B, Schmitt T: Ice-age isolation, postglacial hybridization and recent population bottlenecks shape the genetic structure of Meum athamanticum in Central Europe. Flora. 2012, 207: 399-407. 10.1016/j.flora.2012.03.005.Google Scholar
- Avise JC: Phylogenetic units and currencies above and below the species level. Phylogeny and Conservation. Edited by: Purvis A, Gittleman JL, Brooks T. 2005, Cambridge University Press, New York, 76-101.Google Scholar
- Szymura JM, Uzzell T, Spolsky C: Mitochondrial DNA variation in the hybridizing fire-bellied toads, Bombina bombina and B. variegata. Mol Ecol. 2000, 9: 891-899. 10.1046/j.1365-294x.2000.00944.x.PubMedGoogle Scholar
- Canestrelli D, Cimmaruta R, Costantini V, Nascetti G: Genetic diversity and phylogeography of the Apennine yellowbellied toad Bombina pachypus, with implications for conservation. Mol Ecol. 2006, 15: 3741-3754. 10.1111/j.1365-294X.2006.03055.x.PubMedGoogle Scholar
- Vörös J, Alcobendas M, Martínez-Solano I, García-París M: Evolution of Bombina bombina and Bombina variegata (Anura: Discoglossidae) in the Carpathian Basin: A history of repeated mt-DNA introgression across species. Mol Phylogenet Evol. 2006, 38: 705-718. 10.1016/j.ympev.2005.08.010.PubMedGoogle Scholar
- Hofman S, Spolsky C, Uzzel T, Cogalniceanu D, Babik W, Szymura JM: Phylogeography of the fire-bellied toads Bombina: independent Pleistocene histories inferred from mitochondrial genomes. Mol Ecol. 2007, 16: 2301-2316. 10.1111/j.1365-294X.2007.03309.x.PubMedGoogle Scholar
- Fink S, Excoffier L, Heckel G: Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations. Mol Ecol. 2004, 13: 3501-3514. 10.1111/j.1365-294X.2004.02351.x.PubMedGoogle Scholar
- Nadachowski A: Late Quaternary rodents of Poland with special reference to morphotype dentation analysis of voles. 1982, Panstwowe Wydawnictwo Naukowe, WarszawaGoogle Scholar
- Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu JL: A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol. 2006, 171: 199-221. 10.1111/j.1469-8137.2006.01740.x.PubMedGoogle Scholar
- Magri D: Patterns of post-glacial spread and the extent of glacial refugia of European beech (Fagus sylvatica). J Biogeogr. 2008, 35: 450-463. 10.1111/j.1365-2699.2007.01803.x.Google Scholar
- Litynska-Zajac M: Anthracological analysis. Complex of Upper Palaeolithic sites near, Moravany, Western Slovakia. Edited by: Hromada J, Kozlowski J. 1995, Jagellonian University Press, Krakow, 74-79.Google Scholar
- Willis KJ, Sümegi P, Braun M, Toth A: The late Quaternary environmental history of Bátorliget, NE Hungary. Palaeogeogr Palaeoclimate Palaeoecol. 1995, 118: 25-47. 10.1016/0031-0182(95)00004-6.Google Scholar
- Willis KJ, Rudner E, Sümegi P: The full-glacial forests of Central and southeastern Europe. Quat Res. 2000, 53: 203-213. 10.1006/qres.1999.2119.Google Scholar
- Rudner ZE, Sümegi P: Recurring Taiga forest-steppe habitats in the Carpathian Basin in the Upper Weichselian. Quat Internat. 2001, 76/77: 177-189.Google Scholar
- Sümegi P, Rudner ZE: In situ charcoal fragments as remains of natural wild fires in the upper Würm of the Carpathian Basin. Quat Internat. 2001, 76/77: 165-176.Google Scholar
- Willis KJ, Niklas KJ: The role of Quaternary enviromental change in plant macroevolution: the exception or the rule. Phil Trans R Soc Lond B. 2004, 359: 159-172. 10.1098/rstb.2003.1387.Google Scholar
- Willis KJ, van Andel TH: Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quat Sci Rev. 2004, 23: 2369-2387. 10.1016/j.quascirev.2004.06.002.Google Scholar
- Feurdean A, Wohlfarth B, Björkman L, Tantau I, Bennike O, Willis KJ, Farcas S, Robertsson AM: The influence of refugial population on Lateglacial and early Holocene vegetational changes in Romania. Rev Palaeobot Palynol. 2007, 145: 305-320. 10.1016/j.revpalbo.2006.12.004.Google Scholar
- Normand S, Ricklefs RE, Skov F, Bladt J, Tackenberg O, Svenning JC: Postglacial migration supplements climate in determining plant species ranges in Europe. Proc R Soc B. 2011, 278: 3644-3653. 10.1098/rspb.2010.2769.PubMed CentralPubMedGoogle Scholar
- Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohnty A, Müller-Starck G, Demesure-Musch B, Palmé A, Pedro Martin J, Rendell S, Vendramin GG: Glacial refugia: hotspots but not melting pots of genetic diversity. Science. 2003, 300: 1563-1565. 10.1126/science.1083264.PubMedGoogle Scholar
- Hampe A, Petit RJ: Conserving biodiversity under climate change: the rear edge matters. Ecol Lett. 2005, 8: 461-467. 10.1111/j.1461-0248.2005.00739.x.PubMedGoogle Scholar
- Stewart JR: The evolutionary consequence of the individualistic response to climate change. J Evol Biol. 2009, 22: 2363-2375. 10.1111/j.1420-9101.2009.01859.x.PubMedGoogle Scholar
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