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(American Journal of Botany. 2008;95:1006-1014.) doi: 10.3732/ajb.2007196 © 2008 Botanical Society of America, Inc.

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Trans-Atlantic dispersal and large-scale lack of genetic structure in the circumpolar, arctic-alpine sedge Carex bigelowii s. l. (Cyperaceae)¹

² National Centre for Biosystematics, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway ³ Department of Biogeography and Botanical Garden, Faculty Centre Botany, University of Vienna, A-1030 Vienna, Austria

Received for publication 18 June 2007. Accepted for publication 8 April 2008.

ABSTRACT

Paradoxically, several of the ecologically most important plant groups in the Arctic are little understood in terms of taxonomy and biogeographic history. The circumpolar Carex bigelowii s. l. (Cyperaceae) is abundant in the Arctic and is one of the most complicated arctic plant groups. While its ecology and population genetics have been extensively studied, its taxonomy is largely unexplored. We analyzed the large-scale geographical structuring of amplified fragment length polymorphisms (AFLPs) covering most of the distribution range. We detected high levels of genetic variation, most (66%) within populations, and a fairly weak genetic structure. Only the Central Asian populations, referred to as C. orbicularis, were strongly divergent. For the remaining populations, Bayesian clustering separated three distinct clusters (one European, one amphi-Atlantic, and one broadly amphi-Beringian), probably reflecting different major glacial refugia and recent transoceanic dispersal. The isolated central European populations were most closely related to those from a larger distribution area in northern Europe. Differences in genetic diversity suggest that the Alpine and Tatra populations have experienced strong bottlenecks, whereas the Krkonoe population may have been part of a continuous distribution area during the cold stages of the Pleistocene. Finally, we discuss the relevance of our results for a uniform, range-wide taxonomic concept.

Key Words: AFLP • arctic-alpine flora • Bayesian clustering • Carex bigelowii • Cyperaceae • plant migration • taxonomy

One of the most conspicuous characteristics of arctic taxa is their typically enormous distribution area. The main distribution types in the Arctic are circumpolar, amphi-Atlantic and amphi-Beringian, evident at the species level as well as at more cryptic intraspecific levels (Abbott and Brochmann, 2003). Whereas some arctic plant species are morphologically uniform throughout their range, others have a bewildering amount of variation and have successfully eluded a meaningful range-wide taxonomic treatment. Paradoxically, several of the ecologically most important plant groups in the Arctic are among the ones that are least understood in terms of taxonomy and biogeographic history, such as Dryas (cf. Skrede et al., 2006), Vaccinium (cf. Alsos et al., 2005; Eidesen et al., in press), Draba (cf. Grundt et al., 2004, 2006), and Papaver (cf. Solstad et al., 2003).

Another widespread and ecologically important, but taxonomically complicated arctic species complex is Carex bigelowii Torrey ex Schwein. s. l. where many taxa at or below the species level have been described; 38 are listed in a review by Brooker et al. (2001). The unresolved taxonomy may at least partly be due to the occurrence of numerous partially fertile hybrids (Brooker et al., 2001). The complex presents considerable morphological as well as genetic (Stenström et al., 2001, 2002) variation. However, in some cases, the morphological differences among populations within described taxa have been found to be larger than among differently named taxa (Stenström et al., 2002). Apart from such intrinsic difficulties, the taxonomic problems are probably mainly due to the lack of study of the variation on the full circumpolar scale (Chater, 1980).

Carex bigelowii s. l. has a circumpolar, arctic-alpine distribution (Hultén and Fries, 1986; Fig. 1), surpassing 78° N in Greenland (Böcher et al., 1978) and Svalbard (Elven and Elvebakk, 2002), and is abundant in large parts of the Arctic. Its abundance as well as its occurrence in a wide range of plant communities (Brooker et al., 2001) is an obvious reason that it is one of the best-studied arctic plants in terms of ecology and population genetics. It is self-compatible but seems to be mostly outcrossing; protandry or protogyny limits pollination within flowering shoots (Tikhmenev, 1979; Stenström, 1999). The plants are wind-pollinated, and pollen dispersal over long distances may be facilitated by their preference for wind-exposed and low-growing vegetation. Although the diaspores have no obvious adaptations to dispersal over long distances, they may disperse efficiently when blown over snow (Brooker et al., 2001) or transported internally by birds (Fridriksson, 1968, 1970; Fridriksson and Sigurdsson, 1969). An ability for long-distance dispersal is indicated by colonization of Icelandic lava fields even in the absence of local source populations (Brooker et al., 2001). Carex bigelowii also forms a very long-lived seed bank; studies from both Alaska and Iceland showed that seeds still germinated after c. 200 years (e.g., Vavrek et al., 1991). Seedling recruitment has not, however, been observed in closed vegetation but only occurs in disturbed sites (Jonsson et al., 1996; Stenström, 1999). Indeed, the plants are frequent pioneers on new road verges, fresh river gravel bars, and other initially bare sites, both in mountains and in the Arctic (R. Elven, personal observation in Scandinavia, NE Canada, and Alaska). Once established, they mainly reproduce by clonal growth via rhizomes, and the genets can reach a considerable age. Monoclonal fairy rings on the coast of arctic Siberia were estimated to be >5000 years old (C. arctosibirica; Jonsdottir et al., 2000). Fossil evidence suggests significant historic range shifts because nutlets of C. bigelowii or the closely related (Hendrichs et al., 2004) C. aquatilis dated to 70000–10000 yr BP have been found close to the margin of the last ice sheet on the British Isles, far south of the current distribution (Godwin, 1975).

View larger version (43K): [in this window] [in a new window]   Fig. 1. Map of northern hemisphere with total distribution (broken line; modified from Hultén and Fries, 1986; some isolated northernmost localities were omitted) and sampled populations of Carex bigelowii s. l. and C. orbicularis. The affiliation of the investigated individuals of C. bigelowii s. l. to the three clusters estimated by the program BAPS in a nonspatial clustering of individuals is given as pie-charts. Because of its strong genetic divergence, C. orbicularis (populations 14–16) was not included in the BAPS analysis. See Table 1 for details of the sampled populations.

In spite of its frequent occurrence and abundance in northern tundra vegetation, C. bigelowii is one of the geographically most restricted species in the flora of the Alps, the Carpathians and some small central European mountain ranges (Germany: Harz; Czech Republic/Poland: Krkonoe, Jeseníky). In the Alps, it is confined to a single mountain range (Seetaler Alpen including Saualpe), where it is frequent in low-alpine, dwarf-shrub vegetation (Franz, 2000). All other records mapped by Hultén and Fries (1986) for the Alps are either not confirmed or are rejected as erroneous (H. Niklfeld, University of Vienna, personal communication). In the Carpathians, only a few populations are known from the High Tatras, occurring both in Poland and Slovakia (e.g., Raciborski and Szafer, 1919). Due to their rarity and isolation from the main distribution area, the origin of these central European populations has attracted the interest of botanists for a long time (e.g., Benz, 1922).

Here we explore amplified fragment length polymorphisms (AFLPs) in C. bigelowii s. l. over most of the geographic range to address the phylogeographic history of this complex. The central Asian C. orbicularis Boott 1846, traditionally included in the C. bigelowii complex (e.g., Brooker et al., 2001) but assigned by Egorova (1999) to a separate subsection (Orbiculares T. V. Egorova), was also included. In particular, we address whether there are different genetic groups in this complex reflecting different major glacial refugia and postglacial migration routes and whether the genetic pattern resembles those recently identified in other arctic plant species studied on a circumpolar scale (e.g., Minuartia biflora Schinz & Tell., Ranunculus pygmaeus Wahlenb., Schönswetter et al. [2006b]; Saxifraga oppositifolia L., Abbott et al. [2000]; Vaccinium uliginosum L. s. l., Alsos et al. [2005]; Eidesen et al., in press). Special focus was given to the relationships among the isolated central European populations and those from the main distribution area in the Arctic and adjacent regions (cf. Schönswetter et al., 2003, 2006a, b, 2007) and to the relations across the northern Atlantic Ocean, especially to the possibility for recent trans-Atlantic dispersal, as demonstrated for other plant species (reviewed in Abbott and Brochmann, 2003; Brochmann et al., 2003). Finally, we discuss the implications of the phylogeographic structuring identified in this ecologically important complex for its poorly understood taxonomy, to provide a basis for a later taxonomic revision. For this purpose, we particularly focus on the level of genetic divergence among population groups suggested by some to belong to distinct taxa, such as in central vs. northern Europe, in the eastern vs. western Atlantic regions, within Beringia, and within Siberia.

MATERIALS AND METHODS

Study group
Carex bigelowii Torrey ex Schwein. belongs to section Phacocystis Dumort. This cosmopolitan section contains 70–99 species (Standley et al., 2002), including some widespread northern ones assumed to hybridize with C. bigelowii, e.g., C. acuta L., C. aquatilis Wahlenb. (incl. C. stans Drejer), C. cespitosa L., and C. nigra (L.) Reich. [including C. juncella (Fr.) Th. Fr.]. Here we circumscribe C. bigelowii s. l. in the same way as Egorova (1999) circumscribed the entire subsection Rigidae Fr. ex Kük., thus including C. bigelowii (s. s.), C. rigida Good. non Schrank, C. hyperborea Drejer, C. consimilis T. Holm, C. lugens T. Holm, C. soczavaeana Gorodk., C. ensifolia Turcz. ex V. Krecz., C. rigidioides (Gorodk.) V. Krecz., and C. arctisibirica (Jurtz.) Czerep. We used this wide circumscription as the basis for our sampling because the taxonomic treatments from the last 30 years are mainly regional and differ significantly both as regards to which taxa are accepted and how they are circumscribed. For logistic reasons, we were unable to include material of all described taxa listed in Brooker et al. (2001). We are especially lacking material from the central and eastern Asian mountains, which were less affected by the Pleistocene glaciations than were large parts of the Arctic and may therefore host old, isolated entities (e.g., the type areas of C. rigidioides and C. soczavaeana).

For Europe, Chater (1980) accepted a single species, C. bigelowii, with four subspecies: (1) subsp. bigelowii (incl. C. hyperborea) in northern Europe (also in Greenland and northeastern North America; C. bigelowii was described from New Hampshire and C. hyperborea from Greenland); (2) subsp. rigida Schultze-Motel in central and northwestern Europe including western Fennoscandia, based on Goodenough’s C. rigida described from Scotland and including subsp. nardeticola Holub; (3) subsp. arctisibirica (Jurtz.) Á. Löve & D. Löve in northern Russia (and Siberia), based on a type from Taimyr; and (4) subsp. ensifolia (Gorodk.) Holub in the southern Ural (and Siberia), based on a type from Dahuria.

For Russia, Egorova (1999) accepted three species: C. soczavaeana in northeastern Siberia and Russian Far East (also indicated for Alaska), C. lugens in northeastern Siberia, northern Russian Far East, and northwestern North America (and indicating that C. consimilis is a separate North American species), and C. bigelowii with five subspecies: (1) subsp. bigelowii (including subsp. rigida) in Europe; (2) subsp. rigidioides (Gorodk.) T. V. Egorova in northeastern Siberia, Russian Far East, and Mongolia; (3) subsp. dacica (Heuff.) T. V. Egorova in the central European mountains (Alps to Carpathians) and including Holub’s subsp. nardeticola as concerns the central European plants; (4) subsp. ensifolia throughout Siberia from Ural to Yakutia and Dahuria; and (5) subsp. arctisibirica in arctic European Russia and Siberia east to the Lena and Kolyma rivers. For Siberia, Malyschev in Malyschev and Peschkova (1990) accepted two species: C. bigelowii with two subspecies (subsp. ensifolia [including subsp. arctisibirica] and subsp. rigidioides) and C. lugens (including C. soczavaeana).

For Canada, Scoggan (1978) accepted two species: C. bigelowii in the east and C. lugens (with C. consimilis included with a question mark) in the west, with a slight overlap of ranges in the eastern Mackenzie District and Keewatin District (cf. also Porsild and Cody, 1980). Standley et al. (2002) recognized the same two taxa as subspecies: subsp. bigelowii (incl. C. rigida Good.) and subsp. lugens (T. Holm) T. V. Egorova (including C. consimilis).

For Greenland, Böcher et al. (1978) accepted C. bigelowii with two subspecies: subsp. bigelowii (including C. hyperborea) mainly in the south and west and subsp. nardeticola in the east, the last corresponding to subsp. rigida sensu Schultze-Motel (1968) and Chater (1980).

Sampling, DNA extraction, and AFLP fingerprinting
Leaf material from up to 10 plants from each of 24 populations of C. bigelowii s. l. (Table 1) was sampled in 2003 and 2004 and dried in silica gel. Because of the species’ ability to form large clones, samples were taken as far from each other as possible within the populations. The samples are considered to cover the variation in Europe and around the North Atlantic but leave large gaps, both geographically and with respect to named taxa, in northern Asia and northwestern North America. Voucher specimens (details in Appendix 1) are deposited at the Institute of Botany, University of Vienna (WU), or at the Botanical Museum, University of Oslo (O).

Data analysis
Average gene diversity over loci was calculated and analyses of molecular variance (AMOVAs) were run using the program ARLEQUIN 2.0 (Schneider et al., 1997). The neighbor joining analysis of Nei and Li (1979) genetic distance matrices was done with the program TREECON 1.3b (Van de Peer and De Wachter, 1997). The tree was midpoint rooted. Branch support was estimated with 1000 bootstrap replicates (Felsenstein, 1985).

A population mixture analysis, implemented in the program BAPS v. 4.13 (Bayesian Analysis of Population Structure; Corander et al., 2003, 2004; Corander and Marttinen, 2006, available at http://www.rni.helsinki.fi/jic/bapspage.html), was used to detect population structure by clustering individuals into "panmictic" groups. BAPS performs equally well or even better than the widely used program STRUCTURE (Pritchard et al., 2000) and is 400-fold faster (Corander and Mattinen, 2006). The program treats both the frequencies of the markers and the number of genetically diverged groups as random variables. Stochastic optimization is used to infer the mode of the posterior distribution. Because AFLPs are dominant markers, only AFLP phenotypes can be analyzed, but this procedure does not violate the assumptions of BAPS (Corander et al., 2004). We conducted mixture analysis of both individuals and populations with the geographic origin of the samples either used as informative prior ("spatial clustering of individuals" / "spatial clustering of groups") or not ("clustering of individuals" / "clustering of groups of individuals"). Prior to analysis, samples with identical AFLP phenotypes (putative clones) were removed. BAPS was run with the maximal number of groups (K) set to 2–25 (i.e., a number larger than the number of sampled populations). Each run was replicated six times, and the results were averaged according to the resultant likelihood scores. Because of the distinct divergence of C. orbicularis (populations 14–16) in the neighbor joining analysis (described in Results), these were not included in the BAPS clustering. Population admixture analysis (Corander and Mattinen, 2006) as implemented in BAPS v. 4.13 was employed to unravel the cause of the "misplacement" of three individuals (see Results).

To complement the Bayesian clustering approach with a distance-based phenetic analysis, a principal coordinate analysis (PCoA) based on a matrix of Jaccard distances among individuals was calculated and plotted with the program NTSYS-pc 2.0 (Rohlf, 1997).

RESULTS

In the 209 individuals successfully analyzed, we scored 239 AFLP fragments ranging from 67 to 499 base pairs, of which five were excluded after comparison between the replicated individuals. Among the remaining 234 reproducible AFLP fragments, 230 (98.3%) were polymorphic. The average gene diversity over loci varied from 0.0017 in population 15 (C. orbicularis) to 0.1260 in population 11 from northern Sweden (Table 1). The overall mean was 0.0667 ± 0.0380 SD.

An AMOVA excluding C. orbicularis attributed 34% of the overall variance to variation among the populations, and 66% to the within-population component (Table 2). A nested AMOVA with the three groups of populations obtained in the BAPS analysis (described next) attributed 19% of the overall variance to variation among the three clusters and 19% to variation among populations within the clusters (Table 2).

View larger version (22K): [in this window] [in a new window]   Fig. 2. Principal coordinate analysis (PCoA; first two factors) of all investigated individuals of Carex bigelowii s. l. excluding the divergent central Asian C. orbicularis. The labeling of the individuals is according to the BAPS analysis presented in Fig. 1. Arrows indicate the three individuals with differing cluster affiliation in the four BAPS analyses (see text): 1, one individual of population 10; 2, one individual of population 17; and 3, one individual of population 7.

In the neighbor joining analysis (Fig. 3), two main clades were separated with 100% bootstrap support. One consisted of C. orbicularis from the Altai Mts. (populations 14–16). The other comprised all other accessions and had no well-supported internal branches except for some minor terminal ones.

View larger version (21K): [in this window] [in a new window]   Fig. 3. Neighbor joining analysis of AFLP phenotypes of 209 individuals of Carex bigelowii s. l. and C. orbicularis based on Nei and Li’s (1979) distances. Numbers above branches are bootstrap values higher than 50% (1000 replicates; excluded for groups with <3 AFLP phenotypes). Numbers at the tips of branches are population numbers (Table 1). Individuals with identical AFLP phenotypes are labeled only once if they belong to the same population. Grouping according to the BAPS analyses is indicated (the European, Amphi-Atlantic, and Amphi-Beringian clusters). Arrows indicate the three individuals with differing cluster affiliation in the four BAPS analyses: 1, one individual of population 10; 2, one individual of population 17; and 3, one individual of population 7.

AFLP diversity
Our circumpolar study, in accordance with previous allozyme studies (Jonsson et al., 1996; Stenström et al., 2001), revealed high levels of genetic diversity in populations of C. bigelowii s. l. (Table 1). The structuring of the variation was, however, fairly weak as illustrated by the poor resolution in the neighbor joining analysis (Fig. 3), the low explanatory value of the first two factors in the PCoA (Fig. 2), and the relatively small portion of the global variation explained by differentiation among populations in a nonhierarchical AMOVA (one third; Table 2). Additionally, population admixture analysis (Appendix S1; see Supplemental Data with the online version of this article) suggested gene flow among populations even over enormous distances. This result, though on a much wider geographic scale, is again in accordance with Jonsson et al. (1996), who found low genetic differentiation among three sites of C. bigelowii on Iceland separated by up to 35 kilometers, suggesting extensive gene flow over long distances. Both high variation within populations and weak structuring of the variation are expected for wind-pollinated outcrossers (Hamrick and Godt, 1990). Previous studies with similar sampling design and methodology have revealed much stronger differentiation among populations of wind-pollinated circumpolar arctic-alpine plants. It ranged from 85% of the total genetic variation in Juncus biglumis L. (calculated from the data matrix of Schönswetter et al., 2007) to 93% in Carex atrofusca Schkuhr (calculated from the data matrix of Schönswetter et al., 2006a). The breeding system of J. biglumis is unknown, but the strong differentiation among populations in the cespitose C. atrofusca, as compared to the mainly rhizomatous C. bigelowii s. l., supports the hypothesis that cespitose and rhizomatous growth is associated with predominance of autogamy or allogamy, respectively, in Carex (Jonsson et al., 1996 and references therein).

Large-scale phylogeographical structure
The only clearly divergent genetic lineage in our data set is the central Asian C. orbicularis (populations 14–16). In the neighbor joining analysis (Fig. 3), this taxon was separated from C. bigelowii s. l. with maximal bootstrap support. This separation is in accordance with Egorova (1999), who assigned C. bigelowii and C. lugens to one subsection and C. orbicularis to another. It is also supported by morphology. In C. orbicularis, the female spikes are very dense and subsessile vs. lax to rather dense and shortly pedunculate in C. bigelowii s. l.; the lowest bract is usually shorter than or equal to the spike vs. longer than the spike and sometimes as long as the inflorescence; the utricles are strongly biconvex and sometimes somewhat inflated vs. plano- or slightly biconvex and not inflated; the utricles are distinctly beaked vs. beakless or indistinctly beaked (Egorova, 1999).

In spite of the fairly weak structuring of the genetic variation among the remaining populations, three genetic clusters with different geographic distributions (European, amphi-Atlantic and amphi-Beringian) were revealed by the Bayesian clustering at the individual as well as at the population level (Fig. 1). This structure was also evident in the principle coordinate analysis (Fig. 2) and to a large degree (although with bootstrap support of less than 50%) in the neighbor joining analysis (Fig. 3). Genetic differentiation among the three clusters was fairly weak and accounted for less than 20% of the entire genetic variation (Table 2). The distribution of the European, the Amphi-Atlantic and the Amphi-Beringian clusters partly parallels previously recognized phylogeographic groups, e.g., the European group in Dryas octopetala L. (Skrede et al., 2006) or the amphi-Atlantic and Beringian cpDNA lineages in Vaccinium uliginosum L. (Alsos et al., 2005). Furthermore, the distribution of the three intraspecific groups of C. bigelowii s. l. mirrors frequent distribution patterns at the species level in vascular plants [European cluster: e.g., Chamorchis alpina (L.) Rich., Luzula sudetica DC., Sesleria caerulea (L.) Ard.; Amphi-Atlantic cluster: e.g., Carex arctogena Harry Sm., Sagina caespitosa Lange; Amphi-Beringian cluster: e.g., Cerastium maximum L., Salix rotundifolia Trautv.; Hultén and Fries, 1986; Brochmann et al., 2003].

The enormous distribution of the broadly Amphi-Beringian cluster as well as the strong disjunction of the Amphi-Atlantic cluster across the North Atlantic Ocean (eastern North America, Greenland, Iceland, northern Scandinavia; Fig. 1) argue for extensive dispersal, also over long distances. While we refrain from inferring directions of migrations in the Amphi-Beringian Cluster due to the scarce sampling in that area, some inferences for the Amphi-Atlantic cluster may be drawn. In Europe, this cluster is restricted to the parts of northern Scandinavia that were fully covered by the Weichselian ice sheet until 15000–20000 yr BP, suggesting late glacial or postglacial migration from refugia in eastern North America, south of the Laurentide ice sheet (cf. map in Brochmann et al., 2003). A reduction of genetic diversity due to founder effects during migration was, however, not observed (Table 1). Several previous studies have shown that the North Atlantic was not an important barrier for plant dispersal during and at the end of the last glaciation (reviewed in Abbott and Brochmann, 2003; see also Alsos et al., 2007).

The European and Amphi-Atlantic clusters have at least two contact zones. One of them is on Iceland, where one individual of population 7 was allocated to the Amphi-Atlantic cluster, whereas all other investigated individuals fell into the European cluster. The second meeting zone was encountered in the northern Scandinavian population 10, which was mostly assigned to the European cluster. This population had high levels of admixture (see Appendix S2), resulting in the assignment of one individual to the Amphi-Atlantic cluster in the BAPS analysis at the level of individuals (Fig. 1).

Origin of the central European populations
The central European populations from the eastern Alps, the Krkonoe mountains ("Giant Mountains", at the border of the Czech Republic and Poland) and the High Tatras belong to the European cluster and are thus closely related to the populations from southern/central Scandinavia, Scotland and Iceland. Unfortunately, we were unable to obtain samples from Corsica, the southernmost reported occurrence of C. bigelowii in Europe (Hultén and Fries, 1986).

The neighbor joining analysis (Fig. 3), although weakly structured, suggests multiple migration events between central and northern Europe. A close relationship between the central and northern European populations of a species, though appearing intuitively self-evident and often suggested (e.g., Vierhapper, 1918; Holub, 1968; Ozenda, 1988), has so far been infrequently documented by phylogeographic studies. Good examples for such a connection are Ranunculus glacialis L., which colonized the North Atlantic region from source populations in the eastern Alps (Schönswetter et al., 2003); Dryas octopetala, which colonized northern Europe from source populations located between the Scandinavian ice shield and the Alps (Skrede et al., 2006); and Arabis alpina L., which likely colonized Scandinavia from the Alps (Ehrich et al., 2007). In contrast, in Minuartia biflora (Schönswetter et al., 2006b) and Carex atrofusca (Schönswetter et al., 2006a), the Scandinavian populations formed monophyletic groups, indicating that northern European and Alpine populations have been separated for a certain period of time. Whereas the lack of phylogeographic structure within the four detected phylogeographic groups did not allow us to trace the closest relatives for Alpine and Scandinavian populations of Juncus biglumis (Schönswetter et al., 2007), Ranunculus pygmaeus populations from the last two areas have their closest relatives on the Taymyr Peninsula and in the Urals, respectively (Schönswetter et al., 2006b).

The genetic diversity within populations of C. bigelowii s. l. in the eastern central Alps and the High Tatras was low, indicating bottlenecks during colonization and/or prevalent clonal propagation. Although we tried to minimize sampling of the same clone by collecting plants spread over the entire sampled populations, only three different AFLP phenotypes were observed among the 10 sampled ramets in each of the populations from the Alps (populations 1, 2). In the High Tatras, four and two AFLP phenotypes were detected in 10 and 5 collected individuals, respectively (populations 4, 5). In contrast, in the Krkonoe mountains, each sampled individual represented a distinct AFLP phenotype. Such differences in clonal diversity may indicate that the Alps were reached by a few diaspores only, whereas Krkonoe was part of the main distribution area of C. bigelowii during the cold stages of the Pleistocene. This scenario is supported by the following. (1) The more northern position of Krkonoe as compared to the Alps may imply that the populations in this area were part of a putative continuous population on the tundra covering large parts of central Europe at the maximum of the last glaciation (Frenzel et al., 1992). Fossil evidence (Godwin, 1975) from the British Isles suggests that C. bigelowii (including C. aquatilis that cannot be separated based on fossilized nutlets) was capable of significant historic range shifts, being found far south of its extant distribution on the British Isles. The detection of historic range shifts indirectly supports the presence of C. bigelowii in central Europe during the Pleistocene. (2) The Northern Limestone Alps could have posed a strong barrier for the strictly acidophilic C. bigelowii, preventing direct immigration into the eastern Central Alps from northern source populations. (3) Finally, C. bigelowii is restricted to a single mountain range within the eastern Central Alps. Because this area was the largest unglaciated siliceous portion of the entire Alps (Schönswetter et al., 2005) and presumably provided vast suitable habitats during all stages of the Pleistocene, the local occurrence might suggest that the species has never been more widespread in the Alps. Alternatively, C. bigelowii might have reached the Alps after the Pleistocene via long-distance dispersal. Genets of C. bigelowii can reach a considerable age (>5000 yr; Jonsdottir et al., 2000), and the scarcity of seedling establishment in closed vegetation observed in the north (Jonsson et al., 1996; Stenström, 1999) may suggest a similar situation also for the Alps. It is thus expected that only a few generations may have passed since the end of the last glaciation (c. 14000 yr BP), not leaving enough time for many mutations or extensive recombination to occur. In contrast to the scenario outlined for the Alpine populations, there appears to be no obvious explanation for the reduced level of clonal diversity in the High Tatras.

Taxonomic implications
The results of our phylogeographic analysis of this complex have several obvious taxonomic implications, although final taxonomic conclusions cannot be made without more extensive sampling in northern Asia and northwestern North America and further studies connecting our genetic data to morphological data and inspection of type specimens.

We found no support for differentiation between the central European alpine plants (Egorova’s subsp. dacica) and those of northern and northeastern Europe (mainly subsp. rigida). The proposal of Schultze-Motel (1968), Holub (1968), and Chater (1980) to merge the majority of European plants into one subspecies, for which subsp. rigida is the priority name, is thus supported.

We found that two genetic groups are present in northwestern Europe. Whereas most of the investigated European populations belong to the European cluster, including populations from the type regions of subsp. rigida (Scotland) and subsp. nardeticola (Czech Republic), the northern Swedish population 11 (and parts of populations 7 and 10 from Iceland and northern Sweden) belong to the Amphi-Atlantic cluster. This group also comprises northeastern North American plants, which belong to subsp. bigelowii. The concept of Schultze-Motel (1968) and Chater (1980), who suggested a differentiation into a central and northwestern European subsp. rigida and an amphi-Atlantic subsp. bigelowii, is therefore supported.

The two populations sampled in American Beringia (populations 20 and 21) both belong to the Amphi-Beringian cluster. Obviously, more data from this region are necessary to test a possible separation between C. lugens and C. consimilis (cf. Porsild and Cody, 1980; Standley et al., 2002). However, these two populations are genetically very similar to populations 12–19 sampled in northeastern European Russia and northern Siberia. Although several Siberian taxa were distinguished by Egorova (1999), our results rather suggest that there is a single taxon occurring from northeastern Europe (and Svalbard) across northern Asia to northwestern North America, corresponding to our Amphi-Beringian cluster. Thus, our phylogeographic analysis gave no indication of larger taxonomic variation in the amphi-Beringian region than in the north Atlantic region.

Appendix 1. Taxa used in this study and voucher information. Population numbers are as in Table 1. Voucher specimens are deposited in the following herbaria: Botanical Museum, University of Oslo = O; Institute of Botany, University of Vienna = WU; Polish Academy of Sciences, Kraków = KRAM.

Taxon—Population number: Voucher no., Collector(s), Herbarium, Collection date (day.mo.year).

Carex bigelowii Torrey ex Schwein. s. l.—1, 9135, P. Schönswetter & A. Tribsch, WU, 20.6.2003; 2, 9127, P. Schönswetter & A. Tribsch, WU, 4.7.2003; 3, 9174, L. Schratt-Ehrendorfer, WU, 14.6.2003; 4, Z. Szelag s.n (1996)*, P. Schönswetter & M. Ronikier, KRAM, 26.6.2004; 5, Pawlowski 196310 (1936)*, P. Schönswetter & M. Ronikier, KRAM, 26.6.2004; 6, AK-1325, I. Skrede & P. B. Eidesen, O, 11.8.2003; 7, SUP03-202, SUP03-211, G. Bugge, O, s.d.; 8, SUP03-212, SUP03-230, I. Skrede & H. Jacobsen, O, 28.7.2003; 9, SUP03-155, S. Kjølner & T. Carlsen, O, 18.7.2003; 10, —, K. Winka, —, 2.8.2003; 11, 9342, P. Larson & A. Granberg, O, 27.7.2003; 12, RUS 71, I. G. Alsos & A. Tribsch, O, 23.6.2004; 13, RUS 69, A. Tribsch, O, 5.7.2004; 17, T371, P. Schönswetter & A. Tribsch, WU, 27.7.2004; 18, SUP04-4082, H. Solstad, R. Elven, O, 28.7.2004; 19, SUP04-3891, H. Solstad, R. Elven, O, 12.7.2004; 20, CB-4/63, C. L. Parker, O, 29.7.2004; 21, SUP03-117, H. Solstad, R. Elven, O, 12.8.2003; 22, CB-4/26, I. G. Alsos & A. Brysting, O, 11.8.2004; 23, CA15, I. G. Alsos & A. Brysting, O, 2.8.2004; 24, AK-3044, O. Gilg, O, 25.07.2004.

Carex orbicularis Boott—14, 9559, A. Tribsch, WU, 31.7.2003; 15, 9582, A. Tribsch, WU, 4.8.2003; 16, 9609, A. Tribsch, WU, 7.8.2003.

FOOTNOTES

¹ The authors thank the Austrian Science Fund (Erwin-Schrödinger-Stipend J2311-B03) for financing P. Schönswetter as a postdoctoral fellow at the National Centre for Biosystematics, University of Oslo. Laboratory running costs were covered by the Strategic University Program grant 146515/420 from the Research Council of Norway to C. Brochmann (botany subprogram Migration and evolution of arctic plants in response to Quaternary climate changes). They are most grateful to I. G. Alsos, A. Brysting, P. B. Eidesen, A. K. Brysting, G. Bugge, T. Carlsen, O. Gilg, A. Granberg, G. H. Jacobsen, S. Kjølner, P. Larson, C. L. Parker, M. Ronikier, L. Schratt-Ehrendorfer, I. Skrede, H. Solstad, A. Tribsch, and K. Winka for plant samples. A collecting permit for the Austrian province of Steiermark was issued by the Amt der Steiermärkischen Landesregierung, Fachabteilung 13C (FA13C – 53 S 7/27 – 2003) and permission to collect in the Tatrzaski Park Narodowy (Tatra National Park) was granted to M. Ronikier (permission no. Bot 203). Four anonymous reviewers and C. Fenster provided excellent comments on a previous draft of the manuscript, and C. Dixon improved the English.

⁴ Author for correspondence (e-mail: peter.schoenswetter{at}univie.ac.at)

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