History and evolution of the arctic flora: in the footsteps of Eric Hultén


  • Richard J. Abbott,

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    1. Harold Mitchell Building, Division of Environmental and Evolutionary Biology, School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, UK,
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  • Christian Brochmann

    1. National Centre for Biosystematics/Botanical Garden, The Natural History Museums and Botanical Garden, University of Oslo, PO Box 1172 Blindern, N-0318 Oslo, Norway
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R. J. Abbott. Fax: 01334 463366; E-mail: rja@st-and.ac.uk


A major contribution to our initial understanding of the origin, history and biogeography of the present-day arctic flora was made by Eric Hultén in his landmark book Outline of the History of Arctic and Boreal Biota during the Quarternary Period, published in 1937. Here we review recent molecular and fossil evidence that has tested some of Hultén's proposals. There is now excellent fossil, molecular and phytogeographical evidence to support Hultén's proposal that Beringia was a major northern refugium for arctic plants throughout the Quaternary. In contrast, most molecular evidence fails to support his proposal that contemporary east and west Atlantic populations of circumarctic and amphi-Atlantic species have been separated throughout the Quaternary. In fact, populations of these species from opposite sides of the Atlantic are normally genetically very similar, thus the North Atlantic does not appear to have been a strong barrier to their dispersal during the Quaternary. Hultén made no detailed proposals on mechanisms of speciation in the Arctic; however, molecular studies have confirmed that many arctic plants are allopolyploid, and some of them most probably originated during the Holocene. Recurrent formation of polyploids from differentiated diploid or more low-ploid populations provides one explanation for the intriguing taxonomic complexity of the arctic flora, also noted by Hultén. In addition, population fragmentation during glacial periods may have lead to the formation of new sibling species at the diploid level. Despite the progress made since Hultén wrote his book, there remain large gaps in our knowledge of the history of the arctic flora, especially about the origins of the founding stocks of this flora which first appeared in the Arctic at the end of the Pliocene (approximately 3 Ma). Comprehensive analyses of the molecular phylogeography of arctic taxa and their relatives together with detailed fossil studies are required to fill these gaps.


The present-day arctic flora comprises approximately 1500 species and is of relatively recent origin (Murray 1995). Throughout most of the Tertiary (65–2 Ma), forests grew at high latitudes in the Arctic (Murray 1995; McIver & Basinger 1999) and tundra did not appear until the late Pliocene (Matthews & Ovenden 1990). Initially tundra was distributed discontinuously, but a circumarctic belt was present by 3 Ma (Matthews 1979). Little is known of the origins of arctic plants, although it is supposed that many such plants are derived from ancestral stocks which occurred on high mountains to the south in both Asia and North America (Hultén 1937; Tolmachev 1960; Weber 1965; Hedberg 1992; Murray 1995). These mountains form part of ranges connected to the Arctic, along which plants could have migrated northwards as global temperatures dropped significantly from the mid-Miocene onwards (Lear et al. 2000; Zachos et al. 2001). In addition, some arctic plants may be descended from shrubby and herbaceous elements of the Tertiary arctic forests that occupied open bog, riparian and well-drained upland habitats in the Arctic during the late Tertiary (Murray 1995).

In the Quaternary (approximately 2 Ma until present) the distribution and composition of the arctic flora was greatly affected by the advance and retreat of ice sheets. Traditionally, it was thought that during glacial periods all northern areas were covered by ice to a similar extent and that arctic animals and plants migrated southwards of advancing ice-sheets to survive in southern refugia (Darwin 1859; Hooker 1862). However, this belief was challenged in 1937 by the Swedish botanist, Eric Hultén, in his book Outline of the History of Arctic and Boreal Biota during the Quarternary Period. Hultén drew on geological evidence and a vast body of his own phytogeographical evidence, to propose that most of Northeast Russia and Northwest America (Alaska and the Yukon) remained ice-free during Quaternary glaciations and served as a massive northern refugium for arctic and boreal biota (Fig. 1). Hultén called this region Beringia and defined it as the area between the River Lena (125 E. long.), Northeast Russia, and the River Mackenzie (130 W. long.), Northwest America, and between the Arctic Ocean in the north and southern Alaska and the middle Kuriles in the south. This region served as a land-bridge between Eurasia and North America throughout the Tertiary until approximately 5 Ma when it was severed by the formation of the Bering Strait (Marincovich & Gladenkov 1999, 2001). During the Quaternary, the land-bridge reformed during major glaciations when sea levels fell by 100–135 m (Hopkins 1973; Clark & Mix 2002).

Figure 1.

Distribution of ice cover (white) and tundra (dark grey) in the Northern Hemisphere at the last glacial maximum (after Frenzel 1968; Frenzel et al. 1992). The area defined as Beringia by Hultén (1937) is shown, while margins of exposed continental shelves at the last glacial maximum are indicated by dotted lines.

Hultén further proposed that many arctic plants obtained a circumarctic distribution early in the Quaternary period. However, during each subsequent glaciation, large parts of their distributions were destroyed, only to reform during interglacials through recolonization of deglaciated areas. Some species would have been less successful than others at migrating back into these areas and would retain a fragmented distribution with large gaps occurring between geographically disjunct areas. Extreme examples of such species were those which Hultén described as having an ‘amphi-Atlantic’ or ‘west-Arctic’ distribution, i.e. which occurred on both sides of the Atlantic, but not elsewhere (Hultén 1937, 1958). Hultén argued that these species were exterminated by glaciation throughout most of their former distribution and survived only along the shores of the Atlantic.

In this review, we reconsider Hultén's proposals on the history and evolution of the arctic flora in the light of recent phytogeographical, molecular and fossil evidence. We also examine the traditional view concerning the origin of ancient arctic plants and review molecular evidence which demonstrates that some arctic plant species have originated in relatively recent times. We omit discussion of the evolution and distribution of mating systems and the distribution of ploidy in arctic plants as these aspects have been reviewed elsewhere (Murray 1987, 1995; Brochmann & Steen 1999).

Locations of refugia for arctic plants during Quaternary glaciations

Phytogeographical evidence

Hultén's method for locating glacial refugia for arctic and boreal plants relied on the comparative analysis of the geographical distributions of all known species occurring in Beringia. For approximately 2000 Beringian plant species, he constructed maps of their distribution throughout the Northern Hemisphere. From this large set of maps he selected those of species whose distributions appeared to radiate out in a progressive fashion from a particular location. These were said to occupy ‘equiformal progressive areas’ and form an ‘equiformal progressive series’. Hultén assumed that the region at the core of a particular set of ‘equiformal progressive areas’ was a refugium during glacial times. Those species limited in their distribution to the core were termed ‘centrants’, while those with distributions that radiated out progressively from the core were termed ‘radiants’. Hultén admitted that centrants were selected in an arbitrary manner, while the choice of radiants relied on his assessment of which species distributions neatly fitted into the same set of equiformal progressive areas.

Recently Nimis et al. (1998) reported a phytogeographical analysis of 567 plant species that comprise the flora of the Putorana Plateau in north Siberia. They constructed maps of the geographical distributions of all constituent species, and used numerical analysis to define species groups (chorotypes) based on similar geographical distributions of component species. Maps (chorograms) of each species group were then constructed from the frequency of occurrence of all component species throughout the total distribution of a species group. Their analysis therefore overcame the subjective elements of Hultén's method. Nonetheless, Nimis et al. (1998) identified well-delimited distributional centres for most of the different species groups analysed, and these often corresponded with glacial refugia proposed by Hultén. Beringia was identified as a major glacial refugium for arctic plants, while other refugia for such plants were indicated along the coasts of north Siberia and perhaps in the Putorana Plateau itself.

In addition to proposing that Beringia was a refugium for present-day arctic plants during Quaternary glaciations, Hultén (1937) also suggested that refugia for such plants occurred south of the ice-sheets in Eurasia and North America, and possibly at other locations too. For example, he considered that ice-free areas in the Canadian Arctic Archipelago, north Greenland and the exposed continental shelves of north and west Scandinavia, and north Siberia were all potential refugia as well as the continental shelf of eastern America. Nunataks protruding above the ice in mountain ranges throughout the Northern Hemisphere were other sites mentioned. However, no phytogeographical evidence was provided in support.

The literature providing or reviewing phytogeographical evidence in support of glacial refugia throughout the Northern Hemisphere is now very large, and will not be considered in detail here. For further details see Nordhagen (1936), Dahl (1955, 1987), Löve & Löve (1963; individual chapters in that book), Rønning (1963), Pielou (1991), Birks (1993, 1996, 1997), Birks (1994), Soltis et al. (1997), Bennike (1999), Crawford (1999) and Rundgren & Ingólfsson (1999). The discussion on postulated refugia in the North Atlantic region, in particular in Scandinavia and Svalbard, is revisited below in connection with the origin of the amphi-Atlantic plant distributions.

Phytogeographical evidence of palaeohistorical events must always be treated with caution as the current distribution of plant species will, of course, be also largely affected by present climatic and ecological conditions. Phytogeographical evidence therefore only provides an indication of where glacial refugia were located. Additional evidence for their occurrence may be drawn from studies of molecular geography (Table 1) and fossils.

Table 1.  Molecular evidence for glacial refugia in the Arctic, recent trans-Atlantic or other long distance dispersal of arctic plants, and ancient and recent origins of arctic plants
 SpeciesMolecular evidenceReference
Arctic glacial refugiaCarex spp.IsozymesStenström et al. (2001)
Dryas integrifoliacpDNATremblay & Schoen (1999)
Saxifraga oppositifoliacpDNAAbbott et al. (2000)
Trans-Atlantic dispersalBetula nanacpDNAAlsos, Taberlet & Brochmann (unpubl.)
Cerastium arcticum sensu strictuRAPDs and SCARsHagen et al. (2001)
C. nigrescensRAPDs and SCARsHagen et al. (2001)
Lychnis alpinaIsozymesHaraldsen & Wesenberg (1993)
Phippsia algidaIsozymesAares et al. (2000)
Saxifraga cernuacpDNA and AFLPsBronken et al. (2001)
Saxifraga oppositifoliacpDNAAbbott et al. (2000)
Vaccinium uliginosum subspecies microphyllumcpDNAAlsos et al. (2001); Alsos, Taberlet & Brochmann, unpublished
subspecies uliginosumcpDNAAlsos et al. (2001); Alsos, Taberlet & Brochmann, unpublished
Vahlodea atropurpureaIsozymesHaraldsen et al. (1991)
Other long-distance dispersalDraba alpinaIsozymesBrochmann et al. (1992,1996)
Saxifraga cespitosaRAPDsTollefsrud et al. (1998)
Saxifraga oppositifoliaRAPDsGabrielsen et al. (1997)
Silene acaulisIsozymesAbbott et al. (1995)
Species origins
 AncientSaxifraga oppositifoliacpDNAAbbott et al. (2000)
 RecentSaxifraga osloensiscpDNA and RAPDsBrochmann et al. (1996)
S. svalbardensiscpDNA and RAPDsBrochmann et al. (1998); Brochmann & Håpnes (2001); Steen et al. (2000)
S. opdalensiscpDNA and RAPDsSteen et al. (2000)
Draba spp.IsozymesBrochmann (1992); Brochmann et al. (1992a, 1992b)

Molecular evidence

Molecular evidence is used increasingly to pinpoint the locations of glacial refugia. An important assumption is that present-day populations of a species occurring in areas that were refugia should contain high levels of genetic diversity relative to those occupying deglaciated regions (Hewitt 1996, 2000; Comes & Kadereit 1998; Widmer & Lexer 2001). Neutral genetic diversity is expected to increase in parts of a species distribution that remain intact over a long time period, provided that population size remains large. In contrast, in glaciated areas, only a subsample of this diversity will be present because of frequent founder effects and genetic drift during the recolonization process. An important caveat is that populations occurring in formerly glaciated regions, which are now contact zones between migrants from different refugia, are also likely to contain high levels of genetic diversity. In addition, populations surviving in small glacial refugia such as nunataks are expected to experience drastic reduction in diversity because of genetic drift (Widmer & Lexer 2001).

Surveys of chloroplast DNA RFLP variation in two arctic–alpine species, Dryas integrifolia (Tremblay & Schoen 1999) and Saxifraga oppositifolia (Abbott et al. 2000), have provided the first molecular evidence of Quaternary glacial refugia occurring at high latitudes for such plants. Within D. integrifolia, the phylogeographical pattern of cpDNA variation indicated that at least two major refugia existed in North America throughout the last glaciation (Tremblay & Schoen 1999); one of these was possibly located in Beringia and the other somewhere to the east of this region. However, the phylogeographical signal was not strong and the method of sampling meant that it was difficult to detect regions of higher than average diversity and therefore pinpoint the locations of refugia. Within the circumarctic S. oppositifolia two cpDNA clades were resolved, one of which showed a mainly ‘Eurasian’ distribution, with extensions into Greenland and eastern North America, while the other exhibited a mainly ‘North American’ distribution with extensions into Siberia in the west and north Greenland in the east. The ‘Eurasian’ clade was comprised of four haplotypes (A through D, Fig. 2), and was separated from the ‘North American’ clade (comprised of 10 haplotypes, E–N, Fig. 2) by a minimum of 13 site and length mutations. It is tempting to suggest from this pattern that the species survived the last glaciation in Beringia and migrated out from this refugium in both east and west directions during postglacial times. However, the branch lengths of the two cpDNA clades suggest that they diverged from their common ancestor early in the evolution of S. oppositifolia and have evolved mainly in geographical isolation since then. Furthermore, only haplotypes within the ‘North American’ clade are contained in present-day Beringian material (Fig. 2). Thus, members of the ‘Eurasian’ lineage most probably survived the Quaternary glaciations in Eurasian refugia west of Beringia.

Figure 2.

Geographical distribution of 14 cpDNA haplotypes resolved in Saxifraga oppositifolia. Sector of pie represents the frequency of a particular haplotype in a given region. Haplotypes A, B, C and D comprise the mainly ‘Eurasian clade’, while haplotypes E–N comprise the mainly ‘North American clade’ (Abbott et al. 2000).

Molecular evidence that Beringia was a major refugium for S. oppositifolia during Quaternary glaciations emerges from the high cpDNA haplotype diversity recorded for material sampled from Alaska (Fig. 2; Abbott et al. 2000). High levels of diversity were also recorded in material from the Canadian Arctic Archipelago, north Greenland, west Canada and United States and the Taymyr Peninsula (north Siberia), suggesting that these regions might also have served as refugia at the last glacial maximum. However, high diversity in material from the first three of these regions may simply reflect extensive postglacial colonization by migrants from Beringia. Also, north Greenland is an area of geographical overlap between the two cpDNA clades of S. oppositifolia, and therefore could be a postglacial contact zone for migrants from locations west and east of this region which would inflate diversity. For similar reasons, material sampled from the Taymyr Peninsula may exhibit high diversity. Low cpDNA diversity was evident throughout much of the distribution of the mainly Eurasian lineage of S. oppositifolia, which mainly occupies areas that were heavily glaciated during the Pleistocene (Fig. 1; and Frenzel 1968; Frenzel et al. 1992). One haplotype (A) was fixed in material from Northwest Russia and is common in the Alps and the British Isles, but tends to be replaced by another haplotype (B) in Scandinavia, Svalbard, Iceland, Greenland and east Baffin Island. This geographical structuring might indicate that haplotypes A and B were distributed in different refugia during the last glaciation (and possibly earlier glaciations), from which migrants colonized deglaciated areas in postglacial times. However, it is not possible to tell from this study where these haplotypes survived the glaciation(s), and consequently where glacial refugia occurred for members of the ‘Eurasian’ clade.

Further evidence that plants survived Quaternary glaciations in arctic refugia has come from a recent comparative study of allozyme variation among populations of Carex spp. located at sites along the length of the arctic coast of Eurasia (Stenström et al. 2001). Populations at sites deglaciated ∼10 000 years ago contained significantly less genetic variation than populations from sites that were never glaciated. However, this difference was not independent of variation in species composition between sites and consequently a phylogenetic effect cannot be ruled out.

Additional support for Beringia being a major refugium for arctic organisms comes from surveys of molecular diversity in animals. Several such studies have reported higher levels of genetic diversity in populations of animal taxa sampled from Beringia relative to populations outside the region (Quinn 1992; Bernatchez & Dodson 1994; Weider & Hobæk 1997; Bernatchez & Wilson 1998; Weider et al. 1999a,b; Ehrich et al. 2000; Weider & Hobæk 2002), although this is not always found to be the case (Fedorov et al. 1999; Ehrich et al. 2000).

Fossil evidence

Molecular evidence obtained for both Saxifraga oppositifolia and Dryas integrifolia, although useful in indicating where glacial refugia might have occurred, can often be interpreted in different ways. Fossil evidence, therefore, is normally required to prove that a particular refugium existed. Initial studies of the pollen record for Beringia indicated that during the last glacial maximum it was largely covered by an arctic-steppe or steppe-tundra that was dominated by sagebrush (Artemisia) and grasses (Guthrie 1990). This type of vegetation, for which there is no modern analogue (Hopkins 1967; Murray 1981; Anderson et al. 1989), is believed to have supported populations of large mammals — bison, horse, mammoth — that occurred in Beringia at that time (Guthrie 1968, 1990). More recent fossil evidence, however, has shown that Beringian vegetation was much more heterogeneous during the last glaciation than first thought and, in fact, included a mosaic of different tundra types (Cwynar & Ritchie 1980; Ritchie & Cwynar 1982; Colinvaux & West 1984; Ritchie 1987; Edwards et al. 2000). The first proof that arctic–alpine plants, such as Dryas and Saxifraga species, grew in Beringia at the last glacial maximum came from pollen records for sites in Yukon (Rampton 1971; Cwynar 1982). Subsequently, an analysis of plant and insect macrofossils revealed that lowland, mesic shrub tundra containing plants that occur today in the low Arctic also grew in central parts of the Beringian Land Bridge at the time (Elias et al. 1996, 1997). Recently, an analysis has been conducted of the last full-glacial upland vegetation of part of the northern Seward Peninsula, Central Beringia, Alaska (Goetcheus & Birks 2001), following the discovery that this area was covered by more than 1 m of tephra (volcanic ash) approximately 21 500 bp, and that the former land-surface had been preserved in the permafrost. Detailed macrofossil analysis showed that the vegetation was dry, herb-rich tundra grassland with a continuous moss layer. It contained several plants, including Saxifraga oppositifolia, which are currently widely distributed in the Arctic and in the mountains to the south. This was therefore further proof that Beringia was a refugium for such arctic plants during the last glacial maximum.

A recent analysis of localities in North America where macrofossils of D. integrifolia occur (Tremblay & Schoen 1999) shows that apart from growing in Beringia the species also survived at locations southeast of the North American ice-sheet during the last full glacial period. Other pollen and plant macrofossil records have made clear that tundra occurred at locations to the south, east and west of the ice-sheets in North America (Ritchie 1992; Tremblay & Schoen 1999; Thompson & Anderson 2000) at this time. These refugia, in addition to Beringia, are likely to have been sources of migrants that colonized parts of North America in the immediate postglacial period. In Eurasia, fossil evidence shows that arctic–alpine plants occurred in areas to the south and east of the ice-sheets that covered northern Europe and Northwest Russia during the last glacial maximum (Birks 1994; Tarasov et al. 2000), so it is likely that migrants from these areas, some of which occurred in the Arctic, colonized much of Europe, Northwest Russia, Iceland and Greenland during postglacial times.

Origins of ‘amphi-Atlantic’ and ‘west-Arctic’ plant distributions

The North Atlantic as a barrier to dispersal: hypotheses of Hultén and Dahl

Quite a number of plant species occur disjunctly on both sides of the Atlantic, but are absent from areas eastwards in Eurasia and westwards in North America. Their distributions were mapped in detail by Hultén (1958) in his monumental work The Amphi-Atlantic Plants and their Phytogeographical Connections. The question of how these species crossed the Atlantic, or if they crossed it at all, has been debated continuously in the phytogeographical literature. Of particular interest has been a subset of Hultén's amphi-Atlantic disjuncts, the so-called ‘west-Arctic’ species, which are absent from the Central European mountains. This element contains some 30 species which occur in Scandinavia/Svalbard and in Greenland, with or without extension to continental North America (Dahl 1963, 1987; Nordal 1987). Because the entire current distribution of these species on the European side is situated within the area that was glaciated during the last ice age, the west-Arctic plants have been cited as providing strong evidence in favour of local in situ glacial survival in Scandinavia and Svalbard.

In Hultén's opinion, amphi-Atlantic plants represent the most extremely fragmented remnants of formerly circumpolar species. Hultén proposed that both present-day circumpolar species (for distributions see Hultén 1962, 1971) and amphi-Atlantic species obtained a circumpolar distribution early in the Quaternary via step-wise migration over land, with the two sides of the Atlantic representing endpoints of different migration waves. However, amphi-Atlantic species were exterminated by glaciations throughout most of their former distributions, surviving only along the Atlantic coasts (Hultén 1937, 1958). Thus, according to Hultén's hypothesis, contemporary east and west Atlantic populations of both circumpolar and amphi-Atlantic species have been separated throughout more or less the entire Quaternary.

Hultén regarded the Atlantic Ocean as a virtually inpenetrable barrier against plant dispersal, and particularly so for the amphi-Atlantic species, which he stated had lost their dispersal capacity after repeated isolation and depauperation in small refugial populations. Hultén also rejected an alternative hypothesis of stepwise migration over an Atlantic land bridge, because the floristic similarity between the opposite coasts of the Bering Strait, which had been connected by a land bridge, is much higher than that across the Atlantic.

Other phytogeographers, in particular Dahl (1958, 1963, 1987), agreed with Hultén that the North Atlantic is a strong barrier against plant dispersal. ‘Thus, it is concluded that, whatever is the explanation of the amphi-Atlantic distribution pattern, it is not a matter of long-distance dispersal’ (Dahl 1963 p. 183). Indeed, in contrast to insects, which are highly mobile and rapidly have shifted their distribution ranges in response to the Pleistocene climate oscillations (Coope 1995), it is a fact that the seeds of most arctic–alpine plants lack wings. In Dahl's (1963) analysis of the arctic–alpine flora of Fennoscandia, 70% of 251 species were classified as having ‘no adaptations to long-distance dispersal’, 23% as wind-dispersed (anemochorous), 2% as animal-dispersed (zoochorous), and the remaining species as limnic or halophilous. His anemochorous group included species with very small seeds (< 0.2 mm), or with wings or hairs attached to seeds or fruits. As there was no over-representation of anemochorous or zoochorous species among the west-Arctic or among the other amphi-Atlantic disjuncts, Dahl rejected the hypothesis of long-distance dispersal across the Atlantic. He also rejected, however, Hultén's hypothesis of reductions from former circumpolar ranges, because whereas populations of several polymorphic species or intraspecific taxa occurring on different sides of the Atlantic are very similar, they differ from their closest relatives found further east in Eurasia or further west in America. Dahl (1987) further rejected a hypothesis of postglacial immigration of the amphi-Atlantic species to Scandinavia from the south, partly because there are many more amphi-Atlantic taxa shared among Scandinavia, Iceland and the British Isles than between these areas and the Alps. Thus, by a process of elimination, Dahl (1958, 1963, 1987) explained the amphi-Atlantic disjunctions by postulating stepwise migration across a late Tertiary North Atlantic land bridge and subsequent in situ glacial survival on both sides of the Atlantic during the Quaternary glaciations. The lower degree of floristic similarity across the Atlantic than across the Bering Strait, pointed out by Hultén, was explained by Dahl as a filter effect of this Atlantic land bridge; its ecological conditions allowed only alpine and subalpine species to migrate across.

Thus, although providing different explanations for the origin of the amphi-Atlantic plant distributions, Hultén and Dahl agreed that long-distance seed dispersal across the Atlantic is virtually impossible. They also concluded that the populations occurring on different sides of the Atlantic must have been separated a long time ago and repeatedly survived in different glacial refugia throughout Quaternary glaciations. In the 1960s there was almost complete consensus among phytogeographers that the observed distributions of many arctic–alpine species in Scandinavia and Svalbard could not be explained without postulating in-situ glacial survival, at least during the last glaciation; the alternative possibility of postglacial immigration (the tabula rasa hypothesis) was rejected. In his concluding remarks for the famous Reykjavik Symposium on the North Atlantic Biota and their History, Löve & Löve (1963, p. 391) stated that ‘the theory of glacial survival of plants within glaciated areas of Scandinavia …’ should replace ‘the now merely historical tabula rasa idea’.

Molecular evidence for trans-Atlantic plant dispersal

Other phytogeographers in more recent years, particularly Berg (1963, 1983), Savile (1972) and Nordal (1985a, 1985b, 1987), have argued that long-distance dispersal of arctic–alpine plants may be more common than expected from their lack of specialized dispersal mechanisms. ‘It is obvious that when water cans, doors, and horses may be spread by wind, then may also such seeds and fruits that lack special adaptations to wind dispersal sometimes be lifted and transported by strong winds’ (Berg 1988, translated from Norwegian). In 1987, Nordal re-examined the botanical evidence for the hypothesis of glacial survival and challenged the main conclusion from the Reykjavik symposium (Löve & Löve 1963). She regarded postglacial long-distance dispersal caused by drifting ice, icebergs or birds as the most probable explanation for the amphi-Atlantic disjunctions.

During the last two decades, several studies of plant species occurring in the North Atlantic region have addressed the extent of recent long-distance dispersal using molecular tools (Table 1). Initially, Nordal's group tested her 1987 hypothesis based on allozyme variation in two amphi-Atlantic diploid species. In Vahlodea atropurpurea, which belongs to the west-Arctic subset, no variation was recorded at any of the 17 loci investigated, suggesting a recent bottleneck as well as recent, probably postglacial, dispersal across the Atlantic (Haraldsen et al. 1991). In Lychnis alpina, most diversity was found among populations within geographical regions (such as northern and southern Scandinavia) rather than among populations from different sides of the Atlantic (Haraldsen & Wesenberg 1993). Hagen et al. (2001) presented the first DNA-based analysis (RAPDs and SCARs) of a west-Arctic species, Cerastium arcticum s. lat. This high-polyploid was shown, in fact, to be composed of two highly divergent lineages, which could be recognized as different taxonomic species (C. arcticum s. str. and C. nigrescens; see also Brysting & Borgen 2000; Brysting & Elven 2000). However, although both these lineages are distributed disjunctly across the Atlantic, there is very little geographical structuring of the molecular variation within each lineage. The occurrence of very similar, in some cases even identical, multilocus genotypes of such autogamous high-polyploids on both sides of the Atlantic is caused most probably by postglacial dispersal.

The lack of distinct molecular divergence among populations occurring on different sides of the Atlantic in these amphi-Atlantic species is inconsistent with the expectation under Hultén's and Dahl's hypothesis of long-term isolation during the Quaternary, since at least 2 Ma. Rather, the studies provide strong evidence for recent trans-oceanic migrations, implying that it is no longer necessary to invoke different glacial refugia to explain their current distributions. It is not possible, however, to exclude with certainty the possibility that some populations may have survived on each side of the Atlantic, but the glacial survival hypothesis is not necessary to explain their disjunctions.

Similar, convincing evidence for the existence of more or less continuous gene pools in the entire North Atlantic area has lately accumulated for several circumpolar species, in which according to Hultén (1937, 1958) the contemporary east and west Atlantic populations also should have been separated throughout the Quaternary. In the cpDNA study of S. oppositifolia discussed above (Abbott et al. 2000), the mainly ‘Eurasian clade’ of haplotypes not only extends westwards across the Atlantic; even two closely related haplotypes belong to this clade (A and B, separated by a single mutation) are amphi-Atlantic, both of them occurring in most North Atlantic regions including Scandinavia, Svalbard and eastern continental North America (Fig. 2). In the same species, recent dispersal among three eastern Atlantic regions that commonly have been suggested as different glacial refugia (Svalbard, N and S Scandinavia) was demonstrated using nuclear markers (Gabrielsen et al. 1997). Similar patterns were observed in a recent study of circumpolar cpDNA and AFLP variation in S. cernua (Bronken 2001; Bronken et al. 2001). Also in this species, the North Atlantic region is dominated by two closely related cpDNA haplotypes, and both of them are amphi-Atlantic. Analysis of mainly nuclear AFLP multilocus phenotypes in Saxifraga cernua also indicated considerable intermingling among different areas in the North Atlantic.

Although both of these species of Saxifraga, as well as the amphi-Atlantic species discussed above, are ‘short-distance dispersers’ in the sense of Dahl (1963), they have migrated recently across the Atlantic. In a bird-dispersed circumpolar species, Vaccinium uliginosum, it has now been demonstrated that one of several high-arctic cpDNA haplotypes of the diploid subspecies microphyllum occurs not only across the Atlantic, but has a complete circumpolar distribution (Alsos et al. 2001; Alsos, Taberlet & Brochmann, unpubl. data). Also in the boreal, tetraploid subspecies uliginosum, one haplotype is widespread in Europe and extends across the Atlantic to Greenland, and a closely related haplotype occurs in continental Northeast America. In the wind-dispersed Betula nana, one of the cpDNA haplotypes is found in southern Norway and Svalbard, across the Atlantic to Greenland, and in the Canadian Arctic and Alaska (Alsos, Taberlet & Brochmann, unpubl. data).

Molecular evidence for recent trans-oceanic migrations among various regions in the North Atlantic has also been provided for other species classified as ‘short-distance dispersers’ by Dahl (1963), including the grass Phippsia algida (Aares et al. 2000), Draba alpina (Brochmann et al. 1992, 1996) and yet another species of Saxifraga (S. cespitosa; Tollefsrud et al. 1998). The only deviating pattern identified so far has been found in the tetraploid grass P. concinna, which is virtually fixed for different isozyme multilocus phenotypes in the three main regions analysed (S Norway, Svalbard and Greenland; Aares et al. 2000). It appears there are two alternative, or complementary, explanations for the pattern observed in this hardy snow-bed species. It may have immigrated to southern Norway, Svalbard and Greenland from three different unglaciated source areas, or it may have survived the last glaciation in situ in one or more of these areas.

Complexity of glacial/interglacial phylogeography

The fact that at least several arctic–alpine plant species can disperse over great distances, whether they have specialized dispersal mechanisms or not, certainly does not exclude the possibility that they can have complex and widely differing histories of refugial isolations and range expansions. After examining the disjunct distribution patterns of many arctic–alpine species within Scandinavia, Berg (1963) concluded:

However, most Scandinavian biogeographers explain the arctic–alpine disjunctions in terms of glacial survival … It is my opinion that no single explanation can account for all the arctic–alpine disjunctions in Scandinavia. A great deal of argumentation has resulted from a futile search for the one universal cause. Each species area should be regarded as a problem per se. For future advance to be made in this field, more exact descriptive and experimental data … must be accumulated, species by species.

In fact, molecular studies have shown that species often have different phylogeographical histories, even if they have similar present-day geographical distributions. Although some degree of congruence was observed in Taberlet et al.′s (1998) comparative phylogeographical analysis of temperate European plants and animals, the most striking result was the high degree of incongruence. In the above-mentioned analysis of the snow-bed genus Phippsia (Aares et al. 2000), the two species showed distinctly different phylogeographies in the North Atlantic in spite of their similarity in morphology, habitat ecology, mating system and dispersal ecology. Recent studies of several plant species in the European Alps indicate that their glacial history can be very diverse among as well as within species in this topographically complex area, combining survival on interior nunataks that protruded above the icecap and postglacial immigration from populations surviving outside the ice margin (Stehlik et al. 2001, 2002; Holderegger et al. 2002; Stehlik 2002; 2002). The phylogeographies of arctic animals examined so far appear to show several concordant as well as nonconcordant patterns (Fedorov 1999; Weider & Hobæk 2000). Glacial survival in local Scandinavian refugia was, for example, suggested recently for the Norwegian lemming based on a comparison of mitochondrial DNA variation in this species and in the Siberian lemming (Fedorov & Stenseth 2001).

Hultén showed us that the amphi-Atlantic distribution patterns of plants can be linked, through a series of intermediate patterns, to the fully circumpolar ones. His observation may indeed reflect that some amphi-Atlantic species formerly have had circumpolar ranges. The study of the circumpolar S. oppositifolia (Abbott et al. 2000) supports Hultén's main proposal of range extension from the Beringian/Siberian area towards the west as well as towards the east, although this and other species appear to have continued their migration across the Atlantic.

Origins of arctic plants

Ancient origins

Many plants now found in the Arctic are thought to be derived from ancestors that occurred at high altitudes in mountains to the south during the Tertiary (Hultén 1937, 1958; Tolmachev 1960; Weber 1965; Hedberg 1992). However, there have been few attempts to test this hypothesis (see Murray 1995). As mentioned previously, phylogenetic analysis of cpDNA variation in S. oppositifolia resolved a mainly ‘Eurasian’ clade and a mainly ‘North American’ clade. Interestingly, the two basal haplotypes in each of these clades, haplotypes D and E, respectively, co-occur in the Taymyr region of north Siberia (Fig. 2). A possible explanation for this distribution pattern is that the species first occurred in the Arctic in north Siberia before migrating in east and west directions to obtain a circumpolar distribution. S. oppositifolia is also distributed through the Sino-Himalayan region of central Asia where several other species of Saxifraga sect. Porphyrion subsect. Oppositifoliae occur, which like S. oppositifolia, have opposite leaves (Webb & Gornall 1989; Gornall, unpublished). It is conceivable, therefore, that S. oppositifolia is derived from ancestral stock located in the high mountains of central Asia, which migrated to the Arctic in north Siberia along mountain ranges that connect these two regions. The discovery of late Tertiary macrofossils of S. oppositifolia in the Canadian Arctic Archipelago (Matthews & Ovenden 1990) and in north Greenland (Bennike & Böcher 1990) suggests that migration of the species from north Siberia eastward to north Greenland would have been completed before the start of the Pleistocene. Further molecular phylogenetic analysis is required to confirm that the species with similar morphology which co-occur with S. oppositifolia in the Sino-Himalayan region are indeed its closest relatives, in which case the hypothesis of an origin of S. oppositifolia in this region would be greatly strengthened. Similar studies carried out on other arctic species will determine if the hypothesis of a southern origin at high altitudes during the Tertiary is correct.

Recent origins

The most prominent feature of arctic plant evolution during the Quaternary is complex reticulation. The recent history of the Arctic has been extremely dramatic; its biota have been shaped through numerous large-scale climate changes resulting in cycles of fragmentations, range expansions and reunions of previously isolated populations (Stebbins 1984, 1985). The early Quaternary flora was probably recruited from survivors from the arcto-Tertiary forests combined with immigrants from southern mountain ranges (Murray 1995). This floristic mixture has since been repeatedly spatially rearranged and remixed, and today the majority of arctic plants are hybrids, many of them between plants which themselves are, or were, hybrids. These hybrids have been stabilized by chromosome doubling — allopolyploidization. Successive cycles of divergent evolution among populations isolated in different glacial refugia, migration into deglaciated terrain, hybridization and chromosome doubling have built up increasingly intricate and increasingly high-ploid mixtures. The genes of their diploid or more low-ploid hybrid ancestors are combined into individual plants, each of which carries virtually the entire gene pool of its current population through the next climatic catastrophe. The packing of ancestral genes, originally diversified by divergent evolution, into highly fixed-heterozygous, duplicated genomes ensures that genetic diversity is maintained through periods of extreme inbreeding and bottlenecks, for example when a deglaciated area is recolonized by a single long-distance dispersed seed that establishes a selfing population (Brochmann & Steen 1999).

A recent review of the flora of the isolated arctic archipelago of Svalbard, which was almost completely ice-covered during the last glaciation (Andersen & Borns 1994; Landvik et al. 1998), showed that nearly 80% of the 161 native species are polyploid (Brochmann & Steen 1999). The average ploidal level is close to hexaploid, and quite a few species are very high-ploid. All of the polyploids examined for variation at isozyme loci are fixed-heterozygous, i.e. they are genetically allopolyploid. Most of the few extant diploid species in Svalbard are highly homozygous because of regular self-fertilization, whereas in the polyploids, the level of heterozygosity increases strongly with ploidal level. Thus, the post-Weichselian flora of Svalbard has low species richness in terms of taxonomic species, but these species represent considerable genetic diversity inherited from a much larger stock of diploid ancestral species.

It is well known that the frequency of polyploids is particularly high in the Arctic, but not all polyploids have been formed there. In some groups such as grasses and willows, the original immigrants to the Arctic were already polyploid (Murray 1995). However, many polyploids have certainly been formed in the Arctic throughout the glacial cycles. Because of the repeated cycles of reticulation, however, the detailed evolutionary history of arctic species complexes is extremely difficult to unravel, and it is in many cases impossible to establish a taxonomy and species circumscriptions that correctly reflect their evolutionary history (but see, e.g. Hansen et al. 2000; Fjellheim et al. 2001; Scheen et al. 2002).

A very simple example of polyploid speciation that must almost certainly have taken place after the last glaciation, less than 10 000 years ago, is represented by the allotetraploid, Scandinavian endemic S. osloensis (Brochmann et al. 1996). This species is distributed narrowly in a zone between the currently alpine Scandinavian distribution of the diploid S. adscendens and the lowland distribution of the diploid S. tridactylites. Whereas the cpDNA of S. osloensis is identical to that of S. adscendens, its nuclear multilocus genotypes (RAPDs) can be obtained almost to perfection by adding markers observed in the two diploid species. Thus, the fully sexual and autogamous tetraploid S. osloensis has originated most probably in situ by hybridization between these two diploid species after the last glaciation. The alpine diploid S. adscendens probably immigrated first, after the retreating ice, followed by the more thermophilous diploid S. tridactylites.

Two other narrow endemics in Saxifraga, S. svalbardensis and S. opdalensis, have also probably originated in situ after the last glaciation, but they merely represent the current reticulate endpoints of a far more complex history of reticulate evolution (Brochmann et al. 1998; Gabrielsen & Brochmann 1998; Kjølner et al. 2000; Steen et al. 2000; Brochmann & Håpnes 2001). These species are bulbil-reproducing high polyploids with low but variable levels of fertility, probably caused by aneuploid chromosome numbers. Evidence from a variety of molecular markers suggests that these two species have originated independently via postglacial hybridization between the same two circumpolar species, the octoploid S. rivularis and the variable polyploid S. cernua. Although the same parental species were involved, even with S. rivularis as the maternal parent in both cases, S. svalbardensis and S. opdalensis are morphologically distinct and commonly recognized as different taxonomic species. Their morphological differences probably reflect polymorphisms within one of their parental species, S. cernua; it is likely that two divergent lineages of this variable species were involved in the formation of S. svalbardensis in Svalbard and S. opdalensis in southern Scandinavia.

What, then, are the origins of the parental species themselves? Both of them are allopolyploids, and thus of hybrid origin, as evidenced by fixed heterozygosity at isozyme loci. Their large geographical ranges may indicate that they originated a long time ago. Molecular data suggest that one of the progenitors of the octoploid S. rivularis was S. hyperborea, a widespread arctic tetraploid (cited as diploid in Brochmann et al. 1998; but see Brochmann & Steen 1999). The situation in S. cernua is more complex. This species comprises a range of lineages with different chromosome numbers, some of them even co-occurring at small spatial scales, of which the low-ploid ones may have given and still continue to give rise to the high-ploid ones. Nevertheless, the current, post-Weichselian endemics S. svalbardensis and S. opdalensis have ultimately combined a number of ancestral diploid genomes with different evolutionary histories, inherited via repeated reticulations that have occurred throughout the complex Quaternary history of the arctic flora.

The situation in this group of arctic Saxifraga illustrates a central feature of polyploid speciation — the possibility for multiple origins of a species (see, e.g. Soltis & Soltis 1993, 1999, 2000). The process of hybridization and allopolyploid speciation is simple and rapid, and can be repeated easily in different places at different times, involving more or less divergent populations of the same or even different parental taxonomic species. The end-products of such repeated processes may remain more or less local and ephemeral or become widespread and long-lived, and more or less similar morphologically, so that they may or may not be referred to the same taxonomic species. In the genus Draba, there are some arctic diploids and numerous arctic allopolyploids, up to the 18-ploid level. In this genus, molecular data combined with evidence from morphology and crossing relationships indicate extremely complex evolutionary patterns, ranging from recent, independent and local formation of similar polyploids to multiple origins of widespread, high-polyploid taxa (e.g. Brochmann et al. 1992a, 1992b; summarized in Brochmann 1992). In the genus Saxifraga, the above-mentioned studies not only provided evidence suggesting recurrent formation of the widespread S. cernua itself, but also of polyploids derived from divergent populations of this species and S. rivularis (Brochmann et al. 1998; Steen et al. 2000). In addition to the well-studied endemic polyploids S. opdalensis in southern Norway and S. svalbardensis in Svalbard, there are reports of populations in northern Norway which probably have similar, but independent origins from hybrids between S. cernua and S. rivularis (Rune 1988; Øvstedal 1998; Steen et al. 2000).

Molecular evidence suggesting recurrent formation of arctic–alpine polyploid species has also been obtained in three other genera; Poa (Brysting et al. 1997; 2000), Cerastium (Brysting & Borgen 2000; Hagen et al. 2001), and Dupontia (Brysting et al. 2002). It is now believed that most polyploid plant species are polyphyletic in the sense that they have formed recurrently from genetically divergent diploid progenitors (Soltis & Soltis 2000). This is very evident in the arctic flora, where many diploids and polyploids have enormous and overlapping geographical ranges. Thus, the intriguing taxonomic complexity of the arctic flora — also noted by Hultén — can probably be explained to a large degree by recurrent polyploidizations and subsequent interbreeding of the resulting genotypes.

Divergent evolution at the diploid level in arctic plants can also be more complicated than previously envisioned. In the strongly autogamous diploid Draba fladnizensis, crossing experiments revealed that it consists of at least two sibling species in the North Atlantic (Brochmann et al. 1993). Crosses between morphologically indistinguishable populations of this species from Scandinavia and Svalbard resulted in F1 hybrids that were vigorous and luxuriantly flowering, but entirely sterile. Meiosis was regular, however, indicating that the sterility was caused by minor mutations. Further crossing experiments at the circumpolar scale within this species and within another autogamous diploid, Draba nivalis, have revealed numerous incompatible combinations (Grundt et al. 2001 and unpublished data). It is possible that sibling speciation is a rapid and common process in small and fragmented populations of highly selfing diploids in the Arctic, promoting divergent evolution also within currently recognized taxonomic species. Sibling speciation inhibits mixing of populations that have diverged in different glacial refugia but re-immigrated to the same deglaciated area. Furthermore, it is possible that sibling diploids may occasionally hybridize and form genetically allopolyploid, but taxonomically autopolyploid, derivatives, thus adding yet another level of complexity to arctic plant evolution.

The high proportions of high polyploids and repeated reticulations in many arctic plant groups have previously hampered rigorous analyses of organismal phylogenies based on sequencing of nuclear DNA regions. The best possibility in future projects will be to clone and sequence the various subgenomes of the polyploids and extant diploids, to produce robust phylogenies of all of the constituent diploid genomes present. This approach will make it possible to trace the deep evolutionary and biogeographical history of arctic plants, as well as to map in more detail their more recent reticulations in response to the dramatic climate changes of the Quaternary.


In his various writings on the history and geography of the arctic flora, Eric Hultén (1937, 1958, 1962, 1971, 1973) made numerous proposals on the origin of the present-day flora, patterns of migration and fragmentation of its component species, and the locations of refugia for arctic plants during Quaternary glaciations. These proposals were based on extensive analysis of the phytogeography of arctic plants and an acquired knowledge of the geology of the Arctic. Recent studies using a wide range of molecular, palaeobotanical and phytogeographical approaches have tested several of Hultén's proposals.

There is now excellent fossil, molecular and phytogeographical evidence to support Hultén's proposal that Beringia was a major northern refugium for arctic plants throughout the Quaternary. There is also some suggestive evidence that certain founding stocks of the flora migrated to the Arctic from high mountains located to the south in both Central Asia and North America. These migrations occurred most probably from the mid-Miocene onwards as global temperatures fell dramatically.

Recent molecular evidence, however, has failed to support Hultén's proposals that contemporary east and west Atlantic populations of both circumarctic and amphi-Atlantic species have been separated throughout the entire Quaternary. In fact, populations of arctic plants from each side of the Atlantic are normally genetically very similar to one another. Consequently, the North Atlantic does not appear to have been a barrier to the dispersal of arctic plants throughout the Quaternary, despite the fact that such species do not usually possess obvious characters to promote long-distance dispersal.

Although Hultén did not consider how or whether some arctic plants originated in situ during the Quaternary, Stebbins (1985, 1985) proposed that hybridization and allopolyploidy were important mechanisms of speciation in the Arctic, due to recurrent population fragmentation during glaciations followed by range expansions and secondary contact during interglacials. Molecular evidence has now confirmed that many arctic taxa are allopolyploid, often formed after recurrent polyploidizations, and that several such taxa originated most probably during the Holocene. This mode of evolution probably provides the most important explanation for the intriguing taxonomic complexity of many arctic plant groups. In addition, there is evidence that population fragmentation may lead to the formation of new sibling species at the diploid level.

Despite the considerable progress made in recent years, there remains much to discover about the history and evolution of the arctic flora. We are hopeful that comprehensive analyses of the molecular phylogeny and phylogeography of arctic taxa and their relatives, combined with future fossil discoveries, will continue to build on Eric Hultén's insightful, ground-breaking work, and eventually provide the deep understanding of this flora which Hultén desired.


RJA is grateful to the NERC for supporting his research into the evolutionary history of the arctic flora. CB thanks the Norwegian Research Council for funding his previous and current research on arctic plants. In particular, CB is grateful to all of the former and current members of his research group and to all of his ‘arctic–alpine’ colleagues at the University of Oslo, whose names occur repeatedly in the reference list below.

Dr Richard Abbott investigates various aspects of plant evolution at the University of St Andrews. His current interests focus on the phylogeography of Mediterranean and arctic plants, hybrid speciation and the genetics and evolution of flower head development in the Asteraceae. Professor Christian Brochmann is currently Centre Leader of the National Centre for Biosystematics at the Natural History Museums and Botanical Garden, University of Oslo, where he has recently initiated a 5-year research programme entitled Migration and evolution of arctic plants in response to Quaternary climate change.