Extra-Mediterranean refugia: The rule and not the exception?

ABSTRACT: 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.     

Glacial refugia and postglacial expansion of the alpine–prealpine plant species Polygala chamaebuxus

The shrubby milkwort (Polygala chamaebuxus L.) is widely distributed in the Alps, but occurs also in the lower mountain ranges of Central Europe such as the Franconian Jura or the Bohemian uplands. Populations in these regions may either originate from glacial survival or from postglacial recolonization. In this study, we analyzed 30 populations of P. chamaebuxus from the whole distribution range using AFLP (Amplified Fragment Length Polymorphism) analysis to identify glacial refugia and to illuminate the origin of P. chamaebuxus in the lower mountain ranges of Central Europe. Genetic variation and the number of rare fragments within populations were highest in populations from the central part of the distribution range, especially in the Southern Alps (from the Tessin Alps and the Prealps of Lugano to the Triglav Massiv) and in the middle part of the northern Alps. These regions may have served, in accordance with previous studies, as long‐term refugia for the glacial survival of the species. The geographic pattern of genetic variation, as revealed by analysis of molecular variance, Bayesian cluster analysis and a PopGraph genetic network was, however, only weak. Instead of postglacial recolonization from only few long‐term refugia, which would have resulted in deeper genetic splits within the data set, broad waves of postglacial expansion from several short‐term isolated populations in the center to the actual periphery of the distribution range seem to be the scenario explaining the observed pattern of genetic variation most likely. The populations from the lower mountain ranges in Central Europe were more closely related to the populations from the southwestern and northern than from the nearby eastern Alps. Although glacial survival in the Bohemian uplands cannot fully be excluded, P. chamaebuxus seems to have immigrated postglacially from the southwestern or central‐northern parts of the Alps into these regions during the expansion of the pine forests in the early Holocene.     

The molecular population structure of the tall forb Cicerbita alpina (Asteraceae) supports the idea of cryptic glacial refugia in central Europe

There is an ongoing debate about the glacial history of non‐arctic species in central and northern Europe. The two main hypotheses are: (1) postglacial colonization from refugia outside this region; (2) glacial survival in microclimatically favourable sites within the periglacial areas. In order to clarify the glacial history of a boreo‐montane tall forb, we analysed AFLPs from populations of Cicerbita alpina through most of its range (Scandinavia, the mountains of central Europe, the Alps, the Pyrenees and the Balkan Peninsula). We found a major differentiation between the Pyrenean population and all others, supported by principal coordinate, neighbour joining and STRUCTURE analyses. Furthermore, three populations from the central and north‐eastern Alps were genetically distinct from the bulk of populations from Scandinavia, central Europe, the Alps and the Balkan Peninsula. Most populations, including those from central and northern Europe, had moderate to high levels of genetic diversity (mean Shannon index H_Sh = 0.292, mean percentage of polymorphic loci P = 54.1%, mean Nei's gene diversity H = 0.195). The results indicate separate glacial refugia in the Pyrenean region and the Italian Alps. Furthermore, they provide evidence of glacial persistence in cryptic refugia north of the Alps, from where Scandinavia and most of the Alps are likely to have been colonized following deglaciation. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164 , 142–154.     

Postglacial recolonization in a cold climate specialist in western Europe: patterns of genetic diversity in the adder (Vipera berus) support the central–marginal hypothesis

Understanding the impact of postglacial recolonization on genetic diversity is essential in explaining current patterns of genetic variation. The central–marginal hypothesis (CMH) predicts a reduction in genetic diversity from the core of the distribution to peripheral populations, as well as reduced connectivity between peripheral populations. While the CMH has received considerable empirical support, its broad applicability is still debated and alternative hypotheses predict different spatial patterns of genetic diversity. Using microsatellite markers, we analysed the genetic diversity of the adder (Vipera berus) in western Europe to reconstruct postglacial recolonization. Approximate Bayesian Computation (ABC) analyses suggested a postglacial recolonization from two routes: a western route from the Atlantic Coast up to Belgium and a central route from the Massif Central to the Alps. This cold‐adapted species likely used two isolated glacial refugia in southern France, in permafrost‐free areas during the last glacial maximum. Adder populations further from putative glacial refugia had lower genetic diversity and reduced connectivity; therefore, our results support the predictions of the CMH. Our study also illustrates the utility of highly variable nuclear markers, such as microsatellites, and ABC to test competing recolonization hypotheses.     

Molecular analysis of the Pleistocene history of Saxifraga oppositifolia in the Alps

A recent circumpolar survey of chloroplast DNA (cpDNA) haplotypes identified Pleistocene glacial refugia for the Arctic-Alpine Saxifraga oppositifolia in the Arctic and, potentially, at more southern latitudes. However, evidence for glacial refugia within the ice sheet covering northern Europe during the last glacial period was not detected either with cpDNA or in another study of S. oppositifolia that surveyed random amplified polymorphic DNA (RAPD) variation. If any genotypes survived in such refugia, they must have been swamped by massive postglacial immigration of periglacial genotypes. The present study tested whether it is possible to reconstruct the Pleistocene history of S. oppositifolia in the European Alps using molecular methods. Restriction fragment length polymorphism (RFLP) analysis of cpDNA of S. oppositifolia, partly sampled from potential nunatak areas, detected two common European haplotypes throughout the Alps, while three populations harboured two additional, rare haplotypes. RAPD analysis confirmed the results of former studies on S. oppositifolia; high within, but low among population genetic variation and no particular geographical patterning. Some Alpine populations were not perfectly nested in this common gene pool and contained private RAPD markers, high molecular variance or rare cpDNA haplotypes, indicating that the species could possibly have survived on ice-free mountain tops (nunataks) in some parts of the Alps during the last glaciation. However, the overall lack of a geographical genetic pattern suggests that there was massive immigration of cpDNA and RAPD genotypes by seed and pollen flow during postglacial times. Thus, the glacial history of S. oppositifolia in the Alps appears to resemble closely that suggested previously for the species in northern Europe.     

Multiple cryptic refugia of forest grass Bromus benekenii in Europe as revealed by ISSR fingerprinting and species distribution modelling

Despite not having been fully recognized, the cryptic northern refugia of temperate forest vegetation in Central and Western Europe are one of the most important in the Holocene history of the vegetation on the subcontinent. We have studied a forest grass Bromus benekenii in 39 populations in Central, Western and Southern Europe with the use of PCR-ISSR fingerprinting. The indices of genetic population diversity, multivariate, and Bayesian analyses, supplemented with species distribution modelling have enabled at least three putative cryptic northern refugial areas to be recognized: in Western Europe—the Central and Rhenish Massifs, in Central Europe—the Bohemia–Moravia region and in the Eastern/Western Carpathians. Central Poland is the regional genetic melting-pot where several migratory routes might have met. Southern Poland had a different postglacial history and was under the influence of an Eastern/Western Carpathian cryptic refugium. More forest species should be checked in a west–east gradient in Europe to corroborate the hypothesis on the Western European glacial refugia.     

Higher genetic diversity in recolonized areas than in refugia of Alnus glutinosa triggered by continent‐wide lineage admixture

Genetic admixture is supposed to be an important trigger of species expansions because it can create the potential for selection of genotypes suitable for new climatic conditions. Up until now, however, no continent‐wide population genetic study has performed a detailed reconstruction of admixture events during natural species expansions. To fill this gap, we analysed the postglacial history of Alnus glutinosa, a keystone species of European swamp habitats, across its entire distribution range using two molecular markers, cpDNA and nuclear microsatellites. CpDNA revealed multiple southern refugia located in the Iberian, Apennine, Balkan and Anatolian Peninsulas, Corsica and North Africa. Analysis of microsatellites variation revealed three main directions of postglacial expansion: (i) from the northern part of the Iberian Peninsula to Western and Central Europe and subsequently to the British Isles, (ii) from the Apennine Peninsula to the Alps and (iii) from the eastern part of the Balkan Peninsula to the Carpathians followed by expansion towards the Northern European plains. This challenges the classical paradigm that most European populations originated from refugial areas in the Carpathians. It has been shown that colonizing lineages have met several times and formed secondary contact zones with unexpectedly high population genetic diversity in Central Europe and Scandinavia. On the contrary, limited genetic admixture in southern refugial areas of A. glutinosa renders rear‐edge populations in the Mediterranean region more vulnerable to extinction due to climate change.     

Genetic implications of phylogeographical patterns in the conservation of the boreal wetland butterfly Colias palaeno (Pieridae)

The boreo‐montane wetland butterfly species Colias palaeno has a European distribution from the Alps to northern Fennoscandia. Within its European range, the species’ populations have shrunk dramatically in recent historical times. Therefore, detailed baseline knowledge of the genetic makeup of the species is pivotal in planning potential conservation strategies. We collected 523 individuals from 21 populations across the entire European range and analyzed nuclear (20 allozyme loci) and mitochondrial (600 bp of the cytochrome c oxidase subunit I gene) genetic markers. The markers revealed contrasting levels of genetic diversity and divergence: higher in allozymes and lower in mitochondrial sequences. Five main groups were identified by allozymes: Alps, two Czech groups, Baltic countries, Fennoscandia, and Poland. The haplotype mitochondrial network indicates a recent range expansion. The most parsimonious interpretation for our results is the existence of a continuous Würm glacial distribution in Central Europe, with secondary disjunction during the Last Glacial Maximum into a south‐western and a north‐eastern fragment and subsequent moderate differentiation. Both groups present signs of postglacial intermixing in the Czech Republic. However, even a complete extinction in this region would not considerably affect the species’ genetic basis, as long as the source populations in the Alps and in northern Europe, comprising the most relevant evolutionary units for conservation, are surviving.     

Ice-age isolation,postglacial hybridization and recent population bottlenecks shape the genetic structure of Meum athamanticum in Central Europe

Phylogeographic analyses can help to reveal the refugial structure of plants during and after the ice ages, but the detailed history of regional refugial isolation and differentiation in Central Europe is still poorly understood. A recent study of Meum athamanticum in its total range of occurrences revealed persistence of this temperate montane plant species in Central Europe north of the Alps, without going into details. We therefore aimed to study differentiation and migration processes of this plant species in more detail throughout Central Europe. We used high resolution amplified fragment length polymorphisms (AFLP) markers and analyzed 210 plant individuals of 14 Central European populations with three pairs of primer combinations (128 loci, 111 of which polymorphic). The data show genetic differentiation and varying levels of molecular diversity within populations and groups of populations. Altogether, the studied populations did not show a gradient in molecular variation along presumptive postglacial migration routes across Central Europe. Rather, they reveal a genetic division into seven major groups. Four of them are characterised by high genetic diversity, private fragments and higher than average number of rare and sparse fragments, leading to the assumption that they are descendants of independent populations which survived in glacial refugia. In combination with information from paleoclimate and paleovegetation, it is likely that microclimatically favoured habitats at (i) the eastern flank of the Black Forest, (ii) the southern margin of the Cologne basin, (iii) the foothills of the Erzgebirge, and (iv) the foothills of the Jura Mountains acted as sources for the postglacial recolonisation of this species to the other mountains of Central Europe. As some of the populations analysed show intermixed gene-pools (i.e. including genetic information from different groups) and partly have exceptionally high genetic diversity, but no private and only relatively few rare or sparse fragments, they might represent contact zones. On the other hand, genetic pauperization and isolation of two other populations in connection with extremely small population sizes and unfavourable habitat conditions seem to reflect recent bottlenecks. Consequently, the genetic structure of M. athamanticum in Central Europe is shaped by (i) extra-Mediterranean glacial refugia in situ, (ii) following postglacial hybridization along emerging contact zones and (iii) genetic bottlenecks in thereafter isolated small populations. All results provide evidences for small scale migration of the species between Central European valleys and surrounding highlands. Therefore, our study provides molecular evidence for both climate dependent wide ranging periglacial tabula rasa, but some small refugia in locally buffered areas. We hereby show that the environmental heterogeneity of cold stage landscapes in Central Europe is generally underestimated.     

Galápagos and Californian sea lions are separate species: Genetic analysis of the genus Zalophus and its implications for conservation management

The climatic cycles with subsequent glacial and intergalcial periods have had a great impact on the distribution and evolution of species. Using genetic analytical tools considerably increased our understanding of these processes. In this review I therefore give an overview of the molecular biogeography of Europe. For means of simplification, I distinguish between three major biogeographical entities: (i) "Mediterranean" with Mediterranean differentiation and dispersal centres, (ii) "Continental" with extra-Mediterranean centres and (iii) "Alpine" and/or "Arctic" with recent alpine and/or arctic distribution patterns. These different molecular biogeographical patterns are presented using actual examples. Many "Mediterranean" species are differentiated into three major European genetic lineages, which are due to glacial isolation in the three major Mediterranean peninsulas. Postglacial expansion in this group of species is mostly influenced by the barriers of the Pyrenees and the Alps with four resulting main patterns of postglacial range expansions. However, some cases are known with less than one genetic lineage per Mediterranean peninsula on the one hand, and others with a considerable genetic substructure within each of the Mediterranean peninsulas, Asia Minor and the Maghreb. These structures within the Mediterranean sub-centres are often rather strong and in several cases even predate the Pleistocene. For the "Continental" species, it could be shown that the formerly supposed postglacial spread from eastern Palearctic expansion centres is mostly not applicable. Quite the contrary, most of these species apparently had extra-Mediterranean centres of survival in Europe with special importance of the perialpine regions, the Carpathian Basin and parts of the Balkan Peninsula. In the group of "Alpine" and/or "Arctic" species, several molecular biogeographical patterns have been found, which support and improve the postulates based on distribution patterns and pollen records. Thus, genetic studies support the strong linkage between southwestern Alps and Pyrenees, northeastern Alps and Carpathians as well as southeastern Alps and the Dinaric mountain systems, hereby allowing conclusions on the glacial distribution patterns of these species. Furthermore, genetic analyses of arctic-alpine disjunct species support their broad distribution in the periglacial areas at least during the last glacial period. The detailed understanding of the different phylogeographical structures is essential for the management of the different evolutionary significant units of species and the conservation of their entire genetic diversity. Furthermore, the distribution of genetic diversity due to biogeographical reasons helps understanding the differing regional vulnerabilities of extant populations.     

Species distribution modeling and molecular markers suggest longitudinal range shifts and cryptic northern refugia of the typical calcareous grassland species Hippocrepis comosa (horseshoe vetch)

Calcareous grasslands belong to the most diverse, endangered habitats in Europe, but there is still insufficient information about the origin of the plant species related to these grasslands. In order to illuminate this question, we chose for our study the representative grassland species Hippocrepis comosa (Horseshoe vetch). Based on species distribution modeling and molecular markers, we identified the glacial refugia and the postglacial migration routes of the species to Central Europe. We clearly demonstrate that H. comosa followed a latitudinal and due to its oceanity also a longitudinal gradient during the last glacial maximum (LGM), restricting the species to southern refugia situated on the Peninsulas of Iberia, the Balkans, and Italy during the last glaciation. However, we also found evidence for cryptic northern refugia in the UK, the Alps, and Central Germany. Both species distribution modeling and molecular markers underline that refugia of temperate, oceanic species such as H. comosa must not be exclusively located in southern but also in western of parts of Europe. The analysis showed a distinct separation of the southern refugia into a western cluster embracing Iberia and an eastern group including the Balkans and Italy, which determined the postglacial recolonization of Central Europe. At the end of the LGM, H. comosa seems to have expanded from the Iberian refugium, to Central and Northern Europe, including the UK, Belgium, and Germany.     

Phylogeography of the burnet moth Zygaena transalpina complex: molecular and morphometric differentiation suggests glacial refugia in Southern France,Western France and micro‐refugia within the Alps

Patterns of common recolonization routes from glacial refugia to Central Europe during the Pleistocene are generalized to paradigms of postglacial recolonization in Europe. Recent studies indicate, however, that the actual phylogeographic history of many species might be more complex and cannot be simplified to generalized patterns. Burnet moths of the Zygaena transalpina complex represent a group of closely related taxa, which are considered as a typical example for these generalized patterns. At present, three groups are recognized that are assumed to have spread from three classical refugia in Western Europe, Italy and the Balkans to Central Europe. Here, we re‐investigate their phylogeography using a combined molecular and morphometric approach. Phylogenetic and nested clade phylogeographic analyses of 476 samples from 55 localities taken from Southern and Central Europe reveal that the Zygaena transalpina complex consists of three distinct haplotype clusters, which geographically roughly correspond to possible refugia in Western Europe, Italy and the Balkans. A synthesis of the data with a geometric morphometry dataset of 425 specimens from 46 localities corroborates this molecular result but differs in several aspects. Important new aspects are multiple refugia of the western ‘hippocrepidis’ branch and micro‐habitats within the Alps of the central ‘transalpina’ branch. Further, our results display a more complex phylogeographic pattern for this species complex, which is not tractable with a rigid, generalized pattern.     

Population genomic evidence for plant glacial survival in Scandinavia

Quaternary glaciations have played a major role in shaping the genetic diversity and distribution of plant species. Strong palaeoecological and genetic evidence supports a postglacial recolonization of most plant species to northern Europe from southern, eastern and even western glacial refugia. Although highly controversial, the existence of small in situ glacial refugia in northern Europe has recently gained molecular support. We used genomic analyses to examine the phylogeography of a species that is critical in this debate. Carex scirpoidea Michx subsp. scirpoidea is a dioecious, amphi‐Atlantic arctic–alpine sedge that is widely distributed in North America, but absent from most of Eurasia, apart from three extremely disjunct populations in Norway, all well within the limits of the Weichselian ice sheet. Range‐wide population sampling and variation at 5,307 single nucleotide polymorphisms show that the three Norwegian populations comprise unique evolutionary lineages divergent from Greenland with high between‐population divergence. The Norwegian populations have low within‐population genetic diversity consistent with having experienced genetic bottlenecks in glacial refugia, and host private alleles that probably accumulated in long‐term isolated populations. Demographic analyses support a single, pre‐Weichselian colonization into Norway from East Greenland, and subsequent divergence of the three populations in separate refugia. Other refugial areas are identified in North‐east Greenland, Minnesota/Michigan, Colorado and Alaska. Admixed populations in British Columbia and West Greenland indicate postglacial contact. Taken together, evidence from this study strongly indicates in situ glacial survival in Scandinavia.     

Following the cold: geographical differentiation between interglacial refugia and speciation in the arcto‐alpine species complex Bombus monticola (Hymenoptera: Apidae)

Cold‐adapted species are expected to have reached their largest distribution range during a part of the Ice Ages whereas postglacial warming has led to their range contracting toward high‐latitude and high‐altitude areas. This has resulted in an extant allopatric distribution of populations and possibly to trait differentiations (selected or not) or even speciation. Assessing inter‐refugium differentiation or speciation remains challenging for such organisms because of sampling difficulties (several allopatric populations) and disagreements on species concept. In the present study, we assessed postglacial inter‐refugia differentiation and potential speciation among populations of one of the most common arcto‐alpine bumblebee species in European mountains, Bombus monticola Smith, 1849. Based on mitochondrial DNA/nuclear DNA markers and eco‐chemical traits, we performed integrative taxonomic analysis to evaluate alternative species delimitation hypotheses and to assess geographical differentiation between interglacial refugia and speciation in arcto‐alpine species. Our results show that trait differentiations occurred between most Southern European mountains (i.e. Alps, Balkan, Pyrenees, and Apennines) and Arctic regions. We suggest that the monticola complex actually includes three species: B. konradini   stat.n. status distributed in Italy (Central Apennine mountains), B. monticola with five subspecies, including B. monticola mathildis   ssp.n. distributed in the North Apennine mountains ; and B. lapponicus . Our results support the hypothesis that post‐Ice Age periods can lead to speciation in cold‐adapted species through distribution range contraction. We underline the importance of an integrative taxonomic approach for rigorous species delimitation, and for evolutionary study and conservation of taxonomically challenging taxa.     

Potential source and sink locations for climate‐driven species range shifts in Europe since the Last Glacial Maximum

Aim To identify potential source and sink locations for climate‐driven species range shifts in Europe since the Last Glacial Maximum (LGM). Location Europe. Methods We developed a new approach combining past‐climate simulations with the concept of analogous climate space. Our index gives a continuous measure of the potential of a location to have acted as a source or a sink for species that have shifted their ranges since the LGM. High glacial source potential is indicated by LGM climatic conditions that are widespread now; high post‐glacial sink potential is indicated by current climatic conditions that were widespread at the LGM. The degree of isolation of source and sink areas was calculated as the median distance to areas with analogous climate conditions. Results We identified areas of high glacial source potential in the previously recognized refugial areas in the southern European peninsulas, but also in large areas in central‐western Europe. The most climatically isolated source areas were located in northern Spain, in north‐western Europe and in eastern Turkey. From here species would have had to cover substantial distances to find current climate conditions analogous to LGM conditions of these areas. Areas with high post‐glacial sink potential were mainly located in Fennoscandia and in central and south‐eastern Europe. Some of the most isolated sink areas were located in the Spanish highlands and around the Baltic Sea. Main conclusions Our species‐independent approach successfully identified previously recognized glacial refugial areas with high source potential for species range shifts in southern Europe and in addition highlighted other potential source areas in central Europe. This study offers new insights into how the distribution of past and current climatic conditions may have influenced past species range shifts and current large‐scale biodiversity patterns.     

The origin of unique diversity in deglaciated areas: traces of Pleistocene processes in north‐European endemics from the Galium pusillum polyploid complex (Rubiaceae)

The role of glacial oscillations in shaping plant diversity has been only rarely addressed in endemics of formerly glaciated areas. The Galium pusillum group represents a rare example of an ecologically diverse and ploidy‐variable species complex that exhibits substantial diversity in deglaciated northern Europe. Using AFLP and plastid and nuclear DNA sequences of 67 populations from northern, central, and western Europe with known ecological preferences, we elucidate the evolutionary history of lineages restricted to deglaciated areas and identify the eco‐geographic partitioning of their genetic variation. We reveal three distinct endemic northern lineages: (i) diploids from southern Sweden + the British Isles, (ii) tetraploids from southern Scandinavia and the British Isles that show signs of ancient hybridization between the first lineage and populations from unglaciated central Europe, and (iii) tetraploids from Iceland + central Norway. Available evidence supports a stepwise differentiation of these three lineages that started at least before the last glacial maximum by processes of genome duplication, interlineage hybridization and/or allopatric evolution in distinct periglacial refugia. We reject the hypothesis of more recent postglacial speciation. Ecological characteristics of the populations under study only partly reflect genetic variation and suggest broad niches of postglacial colonizers. Despite their largely allopatric modern distributions, the north‐European lineages of the G. pusillum group do not show signs of rapid postglacial divergence, in contrast to most other northern endemics. Our study suggests that plants inhabiting deglaciated areas outside the Arctic may exhibit very different evolutionary histories compared with their more thoroughly investigated high‐arctic counterparts.     

Phylogeography of a subalpine tall‐herb Ranunculus platanifolius (Ranunculaceae) reveals two main genetic lineages in the European mountains

A phylogeographical analysis of Ranunculus platanifolius, a typical European subalpine tall‐herb species, indicates the existence of two main genetic lineages based on amplified fragment length polymorphism (AFLP) markers. One group comprises populations from the Balkan Peninsula and the south‐eastern Carpathians and the other includes the remaining part of the range of the species, encompassing the western Carpathians, Sudetes, Alps, Pyrenees and Scandinavia. The main phylogeographical break observed in this species runs across the Carpathians and separates the main parts of this range (western and south‐eastern Carpathians), supporting a distinct glacial history of populations in these areas. The high genetic similarity of the Balkan Peninsula and south‐eastern Carpathian populations could indicate a common glacial refugium for these contemporarily isolated areas of species distribution. The western and northern part of the species range displays an additional weak differentiation into regional phylogeographical groups, which could have been shaped by isolation in glacial refugia or even by a postglacial isolation. The observed weak phylogeographical structure could also be linked with ecological requirements, allowing survival along streams in relatively low, forested mountain ranges. © 2013 The Linnean Society of London     

Glacial refugia of mammals in Europe: evidence from fossil records

• 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.

     

Northern glacial refugia for the pygmy shrew Sorex minutus in Europe revealed by phylogeographic analyses and species distribution modelling

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.