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The southern European peninsulas (Iberian, Italian and Balkan) are traditionally recognized as glacial refugia from where many species colonized central and northern Europe after the Last Glacial Maximum (LGM). However, evidence that some species had more northerly refugia is accumulating from phylogeographic, palaeontological and palynological studies, and more recently from species distribution modelling (SDM), but further studies are needed to test the idea of northern refugia in Europe. Here, we take a rarely implemented multidisciplinary approach to assess if the pygmy shrew Sorex minutus, a widespread Eurasian mammal species, had northern refugia during the LGM, and if these influenced its postglacial geographic distribution. First, we evaluated the phylogeographic and population expansion patterns using mtDNA sequence data from 123 pygmy shrews. Then, we used SDM to predict present and past (LGM) potential distributions using two different training data sets, two different algorithms (Maxent and GARP) and climate reconstructions for the LGM with two different general circulation models. An LGM distribution in the southern peninsulas was predicted by the SDM approaches, in line with the occurrence of lineages of S. minutus in these areas. The phylogeographic analyses also indicated a widespread and strictly northern-central European lineage, not derived from southern peninsulas, and with a postglacial population expansion signature. This was consistent with the SDM predictions of suitable LGM conditions for S. minutus occurring across central and eastern Europe, from unglaciated parts of the British Isles to much of the eastern European Plain. Hence, S. minutus likely persisted in parts of central and eastern Europe during the LGM, from where it colonized other northern areas during the late-glacial and postglacial periods. Our results provide new insights into the glacial and postglacial colonization history of the European mammal fauna, notably supporting glacial refugia further north than traditionally recognized.
During the Quaternary ice ages substantial areas of northern Europe were covered by ice sheets while permafrost existed in large areas of central Europe, which restricted the distribution of many temperate and warm-adapted species to the three southern European peninsulas of Iberia, Italy and the Balkans at the Last Glacial Maximum (LGM; Hewitt 2000). These species are interpreted to have recolonized central and northern Europe from these traditionally recognized southern glacial refugia in response to the late-glacial and postglacial warming (Taberlet et al. 1998, Hewitt 2000). Therefore, southern glacial refugia and the northward postglacial recolonization of central and northern Europe from these areas has become an established biogeographical paradigm (Hewitt 2000).
Other studies have, however, provided palaeontological, palynological and phylogeographic evidence that glacial refugia for some temperate and boreal species existed further north than the traditionally recognized southern European refugia, implying a more complex pattern of glacial survival and postglacial recolonization: fossils of temperate mammal species dated to the LGM (albeit rarely small mammals) have been described for a number of sites in central Europe, sometimes in co-occurrence with cold-adapted Pleistocene faunal elements (Sommer and Nadachowski 2006). Macrofossil charcoal (organic plant material≥2 mm in diameter) of coniferous and broad-leaved trees dating to the Upper Palaeolithic has been found in several sites in Austria (42–23 Kya), Czech Republic (29–24.5 Kya), Croatia (27.8–10.8 Kya) and Hungary (31.5–16.5 Kya), suggesting that these regions were also refugial areas for temperate deciduous species (Willis and van Andel 2004, Magri et al. 2006). Palynological records have shown European beech Fagus sylvatica pollen in several sites in central Europe between the late glacial and postglacial (15–10 Kya), and have shown that none of the three traditional refugial areas was the source for northern-central European beech populations (Magri et al. 2006). Phylogeographic studies on several small mammals have shown little similarity between Mediterranean and northern populations, and have described genetic clades linking together haplotypes sampled throughout northern-central Europe (Bilton et al. 1998, Kotlík et al. 2006). Furthermore, species distribution modelling (SDM) has shown that suitable climatic conditions existed for temperate and boreal species in northern latitudes supporting more northerly refugial areas in Europe (Svenning et al. 2008, Fløjgaard et al. 2009). However, a more comprehensive understanding of the relative importance of southern versus northern refugia in terms of LGM species’ ranges as well as for postglacial recolonization is needed.
Here, we use the pygmy shrew Sorex minutus (Mammalia, Soricomorpha), as a model for studying the persistence of populations in northern European refugia during the LGM. Sorex minutus is widely distributed in the Palaearctic, throughout Europe to Lake Baikal (Siberia), including the three southern European peninsulas (Hutterer et al. 2008). The species occurs at low density in a wide range of terrestrial habitats with adequate ground cover (Churchfield and Searle 2008). In southern Europe the distribution becomes patchy and limited to higher altitudes where it occurs with some degree of geographical isolation and differentiation, while in central and northern parts of Europe and in Siberia it is more abundant and populations are more connected and widespread.
Previous phylogeographic studies on S. minutus revealed a very widespread and genetically homogeneous “northern-central European and Siberian” lineage, extending from Britain through central and northern Europe to Siberia (ca 7000 km), but genetically distinct from the southern lineages in Iberia, Italy and the Balkans (Bilton et al. 1998, Mascheretti et al. 2003, McDevitt et al. 2010). These studies suggested that the northern-central European lineage persisted and expanded from one or more central or eastern European refugia located further north than the traditionally recognized southern European refugia. However, the size and locations of the possible northern refugia for S. minutus could not be assessed precisely.
Species distribution models combine information about species occurrences with environmental (usually climatic) data found across the study region to estimate the present-day geographical distribution of suitable environmental conditions for the species (Guisan and Zimmermann 2000). Then, the set of environmental conditions can be projected to past conditions to identify areas where there were suitable environmental conditions for the species (hindcasting) (Nogués-Bravo 2009), in this case at the LGM. Such SDM-based hindcasting has not been integrated into the previous phylogeographic studies on S. minutus, and the genetic data for central and eastern regions of Europe and in Siberia have been rather incomplete. This makes it difficult to determine the importance of these regions for the LGM distribution of the species, its postglacial colonization history and its present-day genetic structure. Moreover, the inference of glacial refugia based solely on phylogeographic analyses can be obscured by the extinction of genetic variants, incomplete sampling and large-scale range shifts of the species (Waltari et al. 2007). Hence at this point, although the previous phylogeographic studies suggested the existence of northern glacial refugia for S. minutus, the size and geographic spread of these refugia as well as their role in the postglacial range dynamics of the species remain unclear.
The purpose of this study is to assess the distribution of S. minutus during the LGM based on a multidisciplinary approach using more detailed mtDNA-based phylogeographic analyses than conducted hitherto and including SDM-based hindcasting. Only a few studies have tried to estimate potential northern refugial areas in this way, despite the stronger inference allowed by these independent and highly complementary approaches (Waltari et al. 2007).
We assessed the following specific study questions: would a more detailed phylogeographic analysis also detect a distinctive “northern-central European and Siberian” lineage as has been previously found? Would this widespread lineage present a genetic signature of population expansion? Would different SDM-based hindcasting approaches predict suitable LGM conditions for S. minutus not only in the southern European peninsulas, but also further north, consistent with northern refugia? Would the combined phylogeographic and SDM approach allow us to estimate more precisely the geographic locations of northern refugia for S. minutus, as well as determine their potential role for its postglacial range dynamics? From the population expansion characteristics, how did the refugial populations colonize their current ranges? Finally, are the rather scant fossil data for S. minutus consistent with our phylogeographic and distributional findings?
This study sheds light on the spatial variation of the genetic diversity within the widespread distribution of S. minutus, its postglacial population expansion and colonization of Europe from northern refugia, and contributes towards an emerging new synthesis of the full-glacial distributions of the European biota. The nature of northern refugia also has important implications for the understanding of their biogeographic roles as sources of genetic diversity, areas of speciation, identification of conservation units and preservation of species, particularly in response to future climate change (Kotlík et al. 2006, Provan and Bennett 2008).
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Specimens and species records of Sorex minutus were made available by several museums and we acknowledge the help of the curators from the following institutions: Dept of Ecology and Evolution (Univ. de Lausanne, Switzerland), Univ. na Primorskem and Research Centre of Koper (Slovenia), Natuurhistorisch Museum (Rotterdam, the Netherlands), Dipartimento di Ecologia (Univ. della Calabria, Italy), Museo di Anatomia Comparata and Museo di Zoologia “La Sapienza” (Univ. di Roma, Italy) and Natuurmuseum Brabant (Tilburg, the Netherlands). We are very grateful for the tissue samples provided by Boris Kryštufec, Allan McDevitt, Glenn Yannic, Jacques Hausser, Jan Zima, Fríða Jóhannesdóttir, Holger Bruns, Peter Borkenhagen and Petr Kotlík. We thank David Nogués-Bravo and two anonymous referees for their valuable comments. Bayesian analyses were run at the Computational Biology Service Unit from Cornell Univ. which is partially funded by Microsoft Corporation. We gratefully acknowledge financial support to R. Vega (181844) and A. Lira-Noriega (189216) from CONACyT (México), and to J.-C. Svenning from the Danish Natural Science Research Council (grant 272-07-0242).This work represents the fruits of the discussion of our work presented at the 4th Biennial Conference of the International Biogeography Society (8–12 January 2009, Mérida, Yucatán, México).