Changing climates during the last 2 million years have profoundly influenced the distribution and abundance of temperate, boreal, and arctic species. Many species have undergone major range shifts in response to changing sea levels or glacial advances and retreats. During the Last Glacial Maximum (LGM) approximately 18,000 years ago, the Fenno-Scandian Ice Sheet in northern Europe and the Laurentide and Cordilleran Ice Sheets in North America extended over large areas of these continents (Ehlers and Gibbard 2007). Many tundra plants nevertheless have broad present-day distributions in both arctic and alpine environments, a pattern which may reflect repeated cycles of expansion, contraction, and migration over several glacial cycles. Molecular studies in combination with fossil evidence have shown diverse phylogeographic patterns among these widespread species, demonstrating how they came to occupy their present ranges and where refugia occurred (Brochmann et al. 2003; Brochmann and Brysting 2008). Both arctic refugia and southern mountain ranges have been suggested as source regions for arctic plants (Murray 1995; Brochmann and Brysting 2008). However, the extent and timelines of contributions to the arctic flora from these different source areas are still not well understood.
Beringia (Yukon to eastern Siberia) provided a large high-latitude ice-free area during the Pleistocene and has long been proposed as a major refugium for many arctic–alpine plant species during glacial periods (Hultén 1937). This hypothesis is well supported by molecular evidence (e.g., Tremblay and Schoen 1999; Abbott et al. 2000; Abbott and Comes 2003; Alsos et al. 2005; Eidesen et al. 2007; Skrede et al. 2009). Although Hultén (1937) considered Beringia the most important refugial region, he suggested that the broad distributions of many tundra species implied dispersal from additional refugia. Many arctic–alpine species persisted in refugia south of continental ice in both Europe and North America (Abbott and Brochmann 2003; Brochmann et al. 2003; Birks 2008; Brochmann and Brysting 2008); examples are Arabis alpina (Koch et al. 2006) and Dryas octopetala (Skrede et al. 2006). Additional refugia may also have existed along glacial margins, in areas such as coastal eastern Greenland (Funder 1979) and coastal British Columbia (Heusser 1989; Ogilvie 1989; Hebda et al. 1997; King et al. 2009). Recent genetic evidence has indicated survival of tundra plant and animal species in unexpected refugia within the overall margins of continental ice sheets of the Late Pleistocene, both in Europe (Westergaard et al. 2011) and in western North America (Loehr et al. 2006; Marr et al. 2008; Shafer et al. 2010a). For tundra plant species, refugia have been suggested in northwestern Europe (Westergaard et al. 2011), northeastern Canada (Tremblay and Schoen 1999), northwestern Canada (Eriksen and Töpel 2006), and northern interior British Columbia (Marr et al. 2008), but further work is needed to determine their overall importance.
Genetic evidence of rapid spread has been found in some arctic–alpine plants. For example, the ranges of Vaccinium uliginosum (Alsos et al. 2005; Eidesen et al. 2007) and Rubus chamaemorus (Ehrich et al. 2008) expanded rapidly following the LGM. Long-distance dispersal and colonization is supported by molecular evidence for a number of arctic species (Brochmann and Brysting 2008), and is the most plausible explanation for current genetic characteristics of many plants found on the remote archipelago of Svalbard (Alsos et al. 2007). However, the potential for rapid migration does not preclude the possibility of survival in multiple locations, including cryptic refugia previously unknown from fossil or palynological evidence (Stewart and Lister 2001; Provan and Bennett 2008). For example, molecular evidence suggests that some European tree species had a more complex glacial history than previously thought, including survival through the LGM in unexpected locations (Birks and Willis 2008). Tundra plants also had complex responses to past climate change (Schönswetter et al. 2005), and may have spread multiple times from steppe or montane habitats (Tkach et al. 2008). An understanding of how dispersal and refugia shaped their present distributions can provide keys to assessing their potential responses to future climate change.
Oxyria digyna Hill is a widespread arctic–alpine perennial herb (Fig. 1) that occurs in tundra habitats over much of the northern hemisphere (Fig. 2), including nearly all of arctic North America and Eurasia and mountain ranges of southern Russia, the Himalayan region, southern Europe, and western North America (Hultén 1971). Its fossil record extends back to the late Tertiary, with macrofossils dated at ∼3 million years reported from arctic Canada (Ellesmere, Meighen, and Prince Patrick Islands, Beaufort Formation; Mathews and Ovenden 1990). It grows in a variety of mesic tundra environments, including scree with little or no soil development. The flowers of Oxyria digyna are inconspicuous and wind-pollinated. The winged seeds are dispersed moderately well by wind (Tackenberg and Stöcklin 2008) and the species establishes effectively on glacial forelands (Whittaker 1993; Stöcklin and Bäumler 1996). Arctic and alpine populations show ecotypic differences in flower and rhizome production and in growth responses to temperature and day length (Mooney and Billings 1961; Heide 2005). Oxyria digyna is taxonomically distinct, with no closely related taxa, and is generally treated as a single well-defined species. Oxyria digyna is largely diploid (2n= 14), with a few hexaploids (2n= 42) reported from Russia (Fedorov 1974; Goldblatt and Johnson 1979–2010).
The history of the tundra floras of the northern hemisphere has been much more extensively investigated in Europe than in North America. In particular, phylogeographic studies of arctic–alpine plants with a focus on western North America are still relatively few (Jorgensen et al. 2003; Bain and Golden 2005), and the contributions of refugia hypothesized for this region (especially cryptic refugia) are not well understood. In a previous study (Marr et al. 2008), we used restriction fragment analysis to identify patterns of genetic diversity in western North American populations of Oxyria digyna in relation to recent glacial history and the locations of refugia. Here we used cpDNA sequence data to reconstruct the broader northern hemisphere phylogeographic history of Oxyria digyna, taking advantage of the much greater power of sequence data to resolve phylogenetic relationships among intraspecific lineages and reveal their early history. We used a combination of analytic approaches together with increased haplotype resolution and greater sampling around the northern hemisphere to address the following questions: (1) what is the geographic structure of genetic variation in Oxyria digyna and how does it compare with other arctic species? (2) How did the species and its major lineages diversify over time and disperse into their present geographic range? (3) What was the contribution of different refugia to the persistence of different lineages in western North America during the LGM?