Glacial refugia of mammals in Europe: evidence from fossil records
Editor: RM
ABSTRACT
- 1
Glacial refugia were core areas for the survival of temperate species during unfavourable environmental conditions and were the sources of postglacial recolonizations. Unfortunately, the locations of glacial refugia of animals and plants are usually described by models, without reference to facts about real geographical ranges at that time.
- 2
Careful consideration of the faunal assemblages of archaeological sites from the Younger Palaeolithic, which are precisely dated to the Last Glacial Maximum (LGM), gives indications about the distribution of species during the LGM (23 000–16 000 bp) and provides evidence for the locations of glacial refugia for mammalian species in Europe.
- 3
In Europe, 47 LGM sites, dating from 23 000 to 16 000 bp and containing typical temperate mammal species, have been described. The geographical range of these archaeological sites clearly shows a distribution which differs from the hypothesized traditional refuge areas of the temperate fauna. A considerable number of sites situated in the Dordogne in south‐western France and the Carpathian region contain records of red deer Cervus elaphus, roe deer Capreolus capreolus, wild boar Sus scrofa and red fox Vulpes vulpes.
- 4
The faunal composition of the majority of the evaluated Palaeolithic sites in the southern European peninsulas (with the exception of Greece), as well as France and the Carpathian region, indicates the co‐occurrence of these temperate species with cold‐adapted faunal elements such as mammoth Mammuthus primigenius and/or reindeer Rangifer tarandus.
- 5
The survival of species in Central European refugia would have significant consequences for phylogeography and would be revealed by the dominant distribution of haplotypes, originating from this region. A Carpathian refuge could also be the reason for the very early records of small mammals or mustelids from the Late‐Glacial or Interstadials before the LGM in regions like southern Germany.
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- ALICE MOUTON, ANDREA GRILL, MAURIZIO SARA, BORIS KRYŠTUFEK, ETTORE RANDI, GIOVANNI AMORI, RIMVYDAS JUŠKAITIS, GAETANO ALOISE, ALESSIO MORTELLITI, FABIANA PANCHETTI and JOHAN MICHAUX, Evidence of a complex phylogeographic structure in the common dormouse, Muscardinus avellanarius (Rodentia: Gliridae), Biological Journal of the Linnean Society, 105, 3, (648-664), (2012).
- Thomas Schmitt and Zoltán Varga, Extra-Mediterranean refugia: The rule and not the exception?, Frontiers in Zoology, 9, 1, (22), (2012).
- P. Colangelo, G. Aloise, P. Franchini, F. Annesi, G. Amori and Jean‐Nicolas Volff, Mitochondrial DNA reveals hidden diversity and an ancestral lineage of the bank vole in the Italian peninsula, Journal of Zoology, 287, 1, (41-52), (2011).
- Emily Lena Jones, Upper Paleolithic rabbit exploitation and landscape patchiness: The Dordogne vs. Mediterranean Spain, Quaternary International, 264, (52), (2012).
- M. Ratkiewicz, M. Matosiuk, R. Kowalczyk, M. K. Konopiński, H. Okarma, J. Ozolins, P. Männil, A. Ornicans, K. Schmidt, Todd Katzner and Jonathan Davies, High levels of population differentiation in Eurasian lynx at the edge of the species' western range in Europe revealed by mitochondrial DNA analyses, Animal Conservation, 15, 6, (603-612), (2012).
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- Ceiridwen J. Edwards, Carl D. Soulsbury, Mark J. Statham, Simon Y.W. Ho, Dave Wall, Gaudenz Dolf, Graziella Iossa, Phillip J. Baker, Stephen Harris, Benjamin N. Sacks and Daniel G. Bradley, Temporal genetic variation of the red fox, Vulpes vulpes, across western Europe and the British Isles, Quaternary Science Reviews, 57, (95), (2012).
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- S. M. Bromilow and F. A. H. Sperling, Phylogeographic signal variation in mitochondrial DNA among geographically isolated grassland butterflies, Journal of Biogeography, 38, 2, (299-310), (2010).
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- Krzysztof SCHMIDT, Mirosław RATKIEWICZ and Maciej K. KONOPIŃSKI, The importance of genetic variability and population differentiation in the Eurasian lynx Lynx lynx for conservation, in the context of habitat and climate change, Mammal Review, 41, 2, (112-124), (2011).
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- Diego J. Álvarez-Lao and Nuria García, Southern dispersal and Palaeoecological implications of woolly rhinoceros (Coelodonta antiquitatis): review of the Iberian occurrences, Quaternary Science Reviews, 30, 15-16, (2002), (2011).
- VANJA BUGARSKI-STANOJEVIĆ, JELENA BLAGOJEVIĆ, GORANA STAMENKOVIĆ, TANJA ADNAĐEVIĆ, EVA B. GIAGIA-ATHANASOPOULOU and MLADEN VUJOŠEVIĆ, Comparative study of the phylogenetic structure in sixApodemusspecies (Mammalia, Rodentia) inferred from ISSR-PCR data, Systematics and Biodiversity, 9, 1, (95), (2011).
- Anna Stankovic, Karolina Doan, Paweł Mackiewicz, Bogdan Ridush, Mateusz Baca, Robert Gromadka, Paweł Socha, Piotr Weglenski, Adam Nadachowski and Krzysztof Stefaniak, First ancient DNA sequences of the Late Pleistocene red deer (Cervus elaphus) from the Crimea, Ukraine, Quaternary International, 245, 2, (262), (2011).
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- Jenni Leppänen, Kari Vepsäläinen and Riitta Savolainen, Phylogeography of the antMyrmica rubraand its inquiline social parasite, Ecology and Evolution, 1, 1, (46), (2011).
- Amber GF Teacher, Jessica A Thomas and Ian Barnes, Modern and ancient red fox (Vulpes vulpes) in Europe show an unusual lack of geographical and temporal structuring, and differing responses within the carnivores to historical climatic change, BMC Evolutionary Biology, 11, 1, (2011).
- Sylvain Dubey and Richard Shine, Plio‐Pleistocene diversification and genetic population structure of an endangered lizard (the Blue Mountains water skink, Eulamprus leuraensis) in south‐eastern Australia, Journal of Biogeography, 37, 5, (902-914), (2010).
- Michal Horsák, Milan Chytrý, Beata M. Pokryszko, Jiří Danihelka, Nikolai Ermakov, Michal Hájek, Petra Hájková, Kateřina Kintrová, Martin Kočí, Svatava Kubešová, Pavel Lustyk, Zdenka Otýpková, Barbora Pelánková and Milan Valachovič, Habitats of relict terrestrial snails in southern Siberia: lessons for the reconstruction of palaeoenvironments of full‐glacial Europe, Journal of Biogeography, 37, 8, (1450-1462), (2010).
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- DAVID STÅHLBERG and MIKAEL HEDRÉN, Evolutionary history of the Dactylorhiza maculata polyploid complex (Orchidaceae), Biological Journal of the Linnean Society, 101, 3, (503-525), (2010).
- Nadia Mucci, Johanna Arrendal, Hermann Ansorge, Michael Bailey, Michaela Bodner, Miguel Delibes, Ainhoa Ferrando, Pascal Fournier, Christine Fournier, José A. Godoy, Petra Hajkova, Silke Hauer, Thrine Moen Heggberget, Dietrich Heidecke, Harri Kirjavainen, Hans-Heinrich Krueger, Kirsti Kvaloy, Lionel Lafontaine, József Lanszki, Charles Lemarchand, Ulla-Maija Liukko, Volker Loeschcke, Gilbert Ludwig, Aksel Bo Madsen, Laurent Mercier, Janis Ozolins, Momir Paunovic, Cino Pertoldi, Ana Piriz, Claudio Prigioni, Margarida Santos-Reis, Teresa Sales Luis, Torsten Stjernberg, Hans Schmid, Franz Suchentrunk, Jens Teubner, Risto Tornberg, Olaf Zinke and Ettore Randi, Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe, Conservation Genetics, 11, 2, (583), (2010).
- Rodrigo Vega, Camilla Fløjgaard, Andrés Lira‐Noriega, Yoshinori Nakazawa, Jens‐Christian Svenning and Jeremy B. Searle, Northern glacial refugia for the pygmy shrew Sorex minutus in Europe revealed by phylogeographic analyses and species distribution modelling, Ecography, 33, 2, (260-271), (2010).
- J. R. Stewart, A. M. Lister, I. Barnes and L. Dalen, Refugia revisited: individualistic responses of species in space and time, Proceedings of the Royal Society B: Biological Sciences, 277, 1682, (661), (2010).
- Juan Manuel López-García, Hugues-Alexandre Blain, Ethel Allué, Sandra Bañuls, Amelia Bargalló, Patricia Martín, Juan Ignacio Morales, Mireia Pedro, Anna Rodríguez, Alex Solé and F. Xavier Oms, First fossil evidence of an “interglacial refugium” in the Pyrenean region, Naturwissenschaften, 97, 8, (753), (2010).
- Patrick Brunet-Lecomte, Armando Nappi and Sophie Montuire, Comparative odontometrical analysis of the first lower molar in Microtus (Terricola) multiplex (Arvicolinae, Rodentia) from western Alps, Acta Theriologica, 55, 2, (129), (2010).
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- G. Cuenca-Bescós, L.G. Straus, J.C. García-Pimienta, M.R. González Morales and J.M. López-García, Late Quaternary small mammal turnover in the Cantabrian Region: The extinction of Pliomys lenki (Rodentia, Mammalia), Quaternary International, 212, 2, (129), (2010).
- Helene Hürner, Boris Krystufek, Maurizio Sarà, Alexis Ribas, Tanja Ruch, Robert Sommer, Victoria Ivashkina and Johan R. Michaux, Mitochondrial phylogeography of the edible dormouse (Glis glis) in the western Palearctic region, Journal of Mammalogy, 91, 1, (233), (2010).
- Miroljub Milenković, Vida Jojić Šipetić, Jelena Blagojević, Svetislav Tatović and Mladen Vujošević, Skull variation in Dinaric–Balkan and Carpathian gray wolf populations revealed by geometric morphometric approaches, Journal of Mammalogy, 91, 2, (376), (2010).
- VALÉRIE DEFFONTAINE, RONAN LEDEVIN, MICHAËL C. FONTAINE, JEAN‐PIERRE QUÉRÉ, SABRINA RENAUD, ROLAND LIBOIS and JOHAN R. MICHAUX, A relict bank vole lineage highlights the biogeographic history of the Pyrenean region in Europe, Molecular Ecology, 18, 11, (2489-2502), (2009).
- R. S. SOMMER, J. M. FAHLKE, U. SCHMÖLCKE, N. BENECKE and F. E. ZACHOS, Quaternary history of the European roe deer Capreolus capreolus, Mammal Review, 39, 1, (1-16), (2008).
- Robert S. Sommer and Frank E. Zachos, Fossil evidence and phylogeography of temperate species: ‘glacial refugia’ and post‐glacial recolonization, Journal of Biogeography, 36, 11, (2013-2020), (2009).
- Camilla Fløjgaard, Signe Normand, Flemming Skov and Jens‐Christian Svenning, Ice age distributions of European small mammals: insights from species distribution modelling, Journal of Biogeography, 36, 6, (1152-1163), (2009).
- Clive Gamble, Human display and dispersal: A case study from biotidal Britain in the Middle and Upper Pleistocene, "Evolutionary Anthropology: Issues, News, and Reviews", 18, 4, (144-156), (2009).
- Michael Hofreiter and John Stewart, Ecological Change, Range Fluctuations and Population Dynamics during the Pleistocene, Current Biology, 19, 14, (R584), (2009).
- Wiesław Bogdanowicz, Ronald A. Van Den Bussche, Marta Gajewska, Tomasz Postawa and Margarita Harutyunyan, Ancient and Contemporary DNA Sheds Light on the History of Mouse-Eared Bats in Europe and the Caucasus, Acta Chiropterologica, 11, 2, (289), (2009).
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- Camilla Fløjgaard, Naia Morueta-Holme, Flemming Skov, Aksel Bo Madsen and Jens-Christian Svenning, Potential 21st century changes to the mammal fauna of Denmark – implications of climate change, land-use, and invasive species, IOP Conference Series: Earth and Environmental Science, 8, (012016), (2009).
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- V. Bugarski‐Stanojević, J. Blagojević, T. Adna?ević, V. Jojić and M. Vujošević, Molecular phylogeny and distribution of three Apodemus species (Muridae, Rodentia) in Serbia, Journal of Zoological Systematics and Evolutionary Research, 46, 3, (278-286), (2008).
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- Jens‐Christian Svenning, Signe Normand and Masa Kageyama, Glacial refugia of temperate trees in Europe: insights from species distribution modelling, Journal of Ecology, 96, 6, (1117-1127), (2008).
- Shonil A. Bhagwat and Katherine J. Willis, Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits?, Journal of Biogeography, 35, 3, (464-482), (2008).
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- R. S. Sommer, When east met west: the sub-fossil footprints of the west European hedgehog and the northern white-breasted hedgehog during the Late Quaternary in Europe, Journal of Zoology, 273, 1, (82), (2007).
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- Eric Waltari, Robert J. Hijmans, A. Townsend Peterson, Árpád S. Nyári, Susan L. Perkins, Robert P. Guralnick and Jerome Chave, Locating Pleistocene Refugia: Comparing Phylogeographic and Ecological Niche Model Predictions, PLoS ONE, 2, 7, (e563), (2007).
- Mirosław Ratkiewicz, Maciej Matosiuk, Alexander P. Saveljev, Vadim Sidorovich, Janis Ozolins, Peep Männil, Linas Balciauskas, Ilpo Kojola, Henryk Okarma, Rafał Kowalczyk, Krzysztof Schmidt and Michael Hofreiter, Long-Range Gene Flow and the Effects of Climatic and Ecological Factors on Genetic Structuring in a Large, Solitary Carnivore: The Eurasian Lynx, PLoS ONE, 10.1371/journal.pone.0115160, 9, 12, (e115160), (2014).
- Elisa Luzi, Piroska Pazonyi and Juan Manuel López‐García, The influence of climate on morphometric traits of fossil populations of Microtus arvalis and M. agrestis from the Carpathian Basin, northern Hungary, Lethaia, , (2018).
- Cristina Fiera, Jan Christian Habel, Mieczysław Kunz and Werner Ulrich, Large‐scale phylogenetic structure of European springtails (Collembola) depends on species range size and postglacial colonization history, Biological Journal of the Linnean Society, , (2016).
- Eli K. Rueness, Sergei Naidenko, Pål Trosvik, Nils Chr. Stenseth and João Pinto, Large-Scale Genetic Structuring of a Widely Distributed Carnivore - The Eurasian Lynx (Lynx lynx), PLoS ONE, 10.1371/journal.pone.0093675, 9, 4, (e93675), (2014).
- Jeremy S. Herman, Fríđa Jóhannesdóttir, Eleanor P. Jones, Allan D. McDevitt, Johan R. Michaux, Thomas A. White, Jan M. Wójcik and Jeremy B. Searle, Post‐glacial colonization of Europe by the wood mouse, Apodemus sylvaticus: evidence of a northern refugium and dispersal with humans, Biological Journal of the Linnean Society, , (2016).
- Piotr Zieliński, Katarzyna Dudek, Michał Tadeusz Stuglik, Marcin Liana, Wiesław Babik and Daniele Canestrelli, Single Nucleotide Polymorphisms Reveal Genetic Structuring of the Carpathian Newt and Provide Evidence of Interspecific Gene Flow in the Nuclear Genome, PLoS ONE, 10.1371/journal.pone.0097431, 9, 5, (e97431), (2014).
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