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Patterns of Endemism and Comparative Phylogeography Confirm Palaeo- Environmental Evidence Forpleistocene Refugia in the Eastern Alps

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Patterns of Endemism and Comparative Phylogeography Confirm Palaeo- Environmental Evidence Forpleistocene Refugia in the Eastern Alps 52 August 2003: 477–497 Tribsch & Schönswetter Pleistocene refugia in E Alps Patterns of endemism and comparative phylogeography confirm palaeo- environmental evidence forPleistocene refugia in the Eastern Alps Andreas Tribsch 1 & PeterSchö nswetter 2 1Department of Higher Plant Systematics and Evolution, Institute of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria. [email protected] (author for correspondence) 2Department of Chorology and Vegetation Science, Institute of Botany, University of Vienna, Rennweg 14, A- 1030 Vienna, Austria. [email protected] Climatic fluctuations during Quaternary glaciations had a significant influence on the distribution of taxa and on their intraspecific genetic structure. In this paper, we test hypotheses on Pleistocene refugia for mountain plants in the eastern part of the European Alps derived from palaeoenvironmental and geological results, with new data on distributional patterns of 288 vascular plant endemics and molecular phylogeographies of select- ed species. High numbers of endemics are found in calcareous regions at the southern and the eastern border of the Eastern Alps, which remained unglaciated during the Pleistocene. The distribution of local endemic taxa in general, and of silicicolous taxa in particular, shows a clear relationship with hypothetical glacial refugia in the southern, southeastern, easternmost, and northeastern Alps. Molecular phylogeographic data from several silicicolous alpine species ( Androsace alpina , Androsace wulfeniana , Eritrichium nanum , Phyteuma globu- lariifolium , Ranunculus glacialis , Saponaria pumila ) are not completely congruent. However, all genetically defined population groups are in congruence with hypothetical refugia. In general, results from distributions of endemic taxa and data from intraspecific phylogeography are compatible with previously hypothesized refu- gia suggesting that refugial situations have shaped the current patterns. The combination of patterns of endemism with molecular phylogeographic data provides an efficacious approach to reveal glacial refugia in vascular plants. KEYWORDS: alpine plants, biogeography, comparative phylogeography, Eastern Alps, endemism, Europe, geology, glacial refugia, Last Glacial Maximum, Pleistocene. vived in disjunct and often geographically restricted INTRODUCTION refugia, possibly resulting in the evolution of genetically It has been early recognised that endemic taxa are distinct lineages. Thus, Pleistocene refugia are regarded not randomly distributed (Candolle, 1875). Range as an important aspect that helped to shape the present restriction as a consequence of survival in refugia has patterns of genetic diversity (Hewitt, 1996; Hugall & al., been regarded as a driving force generating distribution- 2002; Schönswetter & al., 2002; Tribsch & al., 2002). al patterns of endemics. Furthermore, the disruption of Several comparative phylogeographical studies have formerly continuous distributional ranges often results in demonstrated that the ice ages caused partly congruent vicariant speciation (Major, 1988). Arelationship of genetic patterns in several plant and animal species (e.g., areas of high endemism with presumed refugia has been Soltis & al., 1997; Moritz & Faith, 1998; Taberlet & al., documented, e.g., for the Alps (Paw ³ owski, 1970), for 1998; Sullivan & al., 2000). Australia (Crisp & al., 2001) and for Africa (Linder, Ideally, testable biogeographic hypotheses for refu- 2001). However, in most cases, regions were identified gia should be based on independent palaeontological, as refugia based on high levels of endemism or species palaeoenvironmental, and geological evidence. Explicit richness and not based on independent data. studies using this approach have revealed strong rela- Intraspecific genetic patterns, as revealed through tionships of the location of refugia with intraspecific pat- phylogeographic studies, are often strongly influenced terns of phylogeography (Hugall & al., 2002; Nason & by survival of populations during and after glacial peri- al., 2002) or endemism (Tallis, 1991; Crisp & al., 2001). ods. Dramatic climatic changes during the Pleistocene No attempts yet have been made, however, to test caused considerable migration, fragmentation and whether intraspecific phylogeographical patterns are extinction of populations (Hewitt, 1996; Bennett, 1997; congruent with patterns of endemism. If so, these com- Comes & Kadereit, 1998; Dynesius & Jansson, 2000). bined patterns should allow confirmation of the location Taxa, which had formerly continuous distributions, sur- of refugia. 477 Tribsch & Schönswetter Pleistocene refugia in E Alps 52 August 2003: 477–497 In this paper we compare patterns of endemism of vascular plants in the eastern part of European Alps HYPOTHETICAL PLEISTOCENE (Eastern Alps, Fig. 1) with intraspecific phylogeographi- REFUGIA IN THE EASTERN ALPS cal patterns based on molecular data. The Eastern Alps Although the term “refugium” should be used in a provide an appropriate study system, being one of the stringent way (Tallis, 1991), in many studies it is used in best studied mountain areas of the world, with good data different senses (e.g., Hewitt, 1996; Taberlet & al., 1998; on taxonomy, distribution and ecology of the flora, plus Stehlik, 2000). Usually it characterizes regions where detailed geological information (e.g., Vetters, 1933; biota have survived unfavorable climatic conditions. Möbus, 1997). Furthermore, the geological and geomor- Thus, areas with glacial-age fossils are regarded as refu- phological impact of the ice ages has been studied thor- gia, or steep dolomite or serpentine slopes hosting “refu- oughly (e.g., Penck & Brückner, 1909; Jäckli, 1970; gial” populations of plants growing otherwise in high Nagl, 1972; van Husen, 1987, 1997). The extent of the altitudes above tree line. If we focus on long-term sur- last glacial advances, especially during the Würm-glacia- vival, e.g., throughout the last glaciation and Holocene, tion, and the altitudinal fluctuations of the snowline are only those populations that survived cold periods and known in detail, providing geological evidence for gave rise to new populations in warm periods (and vice potential glacial refugia. Additionally, several palaeonto- versa) should be regarded as refugial (see Haffer, 1982; logical studies have focused on the vegetational history Tallis, 1991). An ideal refugium, therefore, prevents of the Eastern Alps and adjacent forelands (e.g., Frenzel, extinction and functions as a genetic reservoir by provid- 1964; Bortenschlager, 1972; Bennett & al., 1991; Foddai ing habitats for survival of plant populations during slow & Minelli, 1994; Lang, 1994; Burga & Perret, 1998; and abrupt climatic changes. Moscariello & al., 2000). All these data are useful in We define a refugium as a geographical area of rela- helping to interpret organismic shifts and reconstruct the tive ecological stability that provided habitats during climate and past environments. cold and warm, wet and dry stages during the Quaternary We first summarize palaeo-environmental, palaeon- for survival of populations, more or less in situ. Thus, a tological, and geological data for the Eastern Alps. Based refugium was (more or less) situated in the same place on this information, we delimit potential refugia within during all stages of the Quaternary, for example, in the Eastern Alps. We then test whether the hypothetical mountain ranges that never have been fully glaciated. In refugia are also centers of endemism and whether genet- such refugia, local migrations in response to climatic ically differentiated groups of populations occur there. changes were mainly vertical. Within a refugium, there- fore, similar climatic and edaphic conditions must be present during climatic change to assure survival of pop- ulations. Fig. 1. The Eastern European Alps. Elevation: above 900 m (light grey), above 2100 m (dark grey); borders of countries are given by yellow lines; dashed line indicates border between the Western and Eastern Alps. 478 52 August 2003: 477–497 Tribsch & Schönswetter Pleistocene refugia in E Alps It has been predicted and demonstrated that moun- of the Eastern Alps is between 3400 and 3500 m (approx- tain areas in general are important refugial areas (Bennett imately 300 m above snowline; Reisigl & Pitschmann, & al., 1991; Tzedakis, 1993; Hewitt, 1996; Taberlet & 1958; Körner, 1999; A. Tribsch & P. Schönswetter, pers. Cheddadi, 2002). Because of high habitat diversity in observ.). mountain areas, not only alternations of cold and warm Despite the possibility that alpine plants could have periods, but also of wetter and drier periods, are easily survived the LGM on nunataks within the Alps, the buffered which guarantees long-term ecological stability. extent and importance of nunatak survival are still under Lowland habitats without direct connections to moun- discussion (Stehlik, 2000; Gugerli & Holderegger, 2001; tains cannot be regarded as refugia for mountain plants, Tribsch & al., 2002; Stehlik, 2003). In principle, there because the ecological conditions were not stable over were thousands of ice-free nunatak areas, at least on time. exposed ridges and southern slopes even in heavily glaciated central parts of the Eastern Alps (central nunataks; Schönswetter & al., 2002). Only a few regions (e.g., Salzburger Schieferalpen, Kitzbühler Alpen and PALAEO-ENVIRONMENTAL, Nonsberggruppe) were completely covered with ice dur- PALAEONTOLOGICAL,
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