Late Pleistocene origin of the entire circumarctic range of the arctic‐alpine plant Kalmia procumbens

Abstract

The circumarctic ranges of arctic-alpine plants are thought to have been established in the late Pliocene/early Pleistocene, when the modern arctic tundra was formed in response to climate cooling. Previous findings of range-wide genetic structure in arctic-alpine plants have been thought to support this hypothesis, but few studies have explicitly addressed the temporal framework of the genetic structure. Here, we estimated the demographic history of the genetic structure in the circumarctic Kalmia procumbens using sequences of multiple nuclear loci and examined whether its genetic structure reflects prolonged isolation throughout the Pleistocene. Both Bayesian clustering and phylogenetic analyses revealed genetic distinction between alpine and arctic regions, whereas detailed groupings were somewhat discordant between the analyses. By assuming a population grouping based on the phylogenetic analyses, which likely reflects a deeper intraspecific divergence, we conducted model-based analyses and demonstrated that the intraspecific genetic divergence in K. procumbens likely originated during the last glacial period. Thus, there is no need to postulate range separation throughout the Pleistocene to explain the current genetic structure in this species. This study demonstrates that range-wide genetic structure in arctic-alpine plants does not necessarily result from the late Pliocene/early Pleistocene origin of their circumarctic ranges and emphasizes the importance of a temporal framework of the current genetic structure for understanding the biogeographic history of the arctic flora.

East Asian origin of the widespread alpine snow‐bed herb, Primula cuneifolia (Primulaceae), in the northern Pacific region

“…Rhodiola integrifolia in Guest & Allen, 2014; Bistorta vivipara in Marr et al., 2013) and the Arctic (e.g. Cassiope tetragona in Eidesen, Carlsen, Molau, & Brochmann, 2007; Kalmia procumbens in Ikeda et al., 2017; Arctic char in Moore, Bajno, Reist, & Taylor, 2015; Saxifraga oppositifolia in Winkler et al., 2012). Furthermore, other studies have inferred that boreal trees persisted in the Kamchatka Peninsula, and were unlikely to colonize northward from southern ranges (Aizawa et al., 2007; Polezhaeva, Lascoux, & Semerikov, 2010).…”

“…Because there is no specific substitution rate in P . cuneifolia , we assumed 5.3–7.8 × 10 –9 substitutions per site per year to scale the divergence time following our previous studies (Hata et al., 2017; Ikeda et al., 2017, 2018) based on spontaneous mutation rates in Arabidopsis thaliana mutation accumulation lines (Ossowski et al., 2010).…”

“…alpine as well as arctic–alpine plants survived in ice‐free refugia south of continental ice sheets (Schönswetter, Paun, Tribsch, & Niklfeld, 2003; Schönswetter et al., 2005), mountain tops within ice sheets (Allen, Marr, McCormick, & Hebda, 2015; Marr, Allen, Hebda, & McCormick, 2013; Stehlik, Blattner, Holderegger, & Bachmann, 2002; Westergaard et al., 2011) and Beringia (far eastern Russia and portions of Alaska and the Yukon, as well as the Bering Land Bridge; Beringia; Abbott, 2000; Abbott & Brochmann, 2003; Eidesen et al., 2013), from which they spread to their current distributions. Several studies have inferred the persistence of isolated populations on high mountains at the southern range margins in North America (Allen, Marr, McCormick, & Hebda, 2012; Allen et al., 2015; Marr et al., 2013), Europe (Eidesen et al., 2013; Ikeda et al., 2017) and the central part of Japan (Ikeda, Higashi, Yakubov, Barkalov, & Setoguchi, 2014; Ikeda, Senni, Fujii, & Setoguchi, 2006, 2008). These marginal populations harbour unique genetic variation; therefore, the importance of southern mountain ranges for the evolution of cold‐adapted plants has been discussed (Winkler et al., 2012).…”

“…Phylogeographic studies have revealed unique genetic divergence in populations in central Japan, implying that alpine plants in Japan persisted during several cycles of the Pleistocene climate changes after their colonization (e.g, Ikeda, Fujii, & Setoguchi, 2009; Ikeda et al., 2014; Ikeda, Senni, Fujii, & Setoguchi, 2006; Ikeda, Senni, Fujii, & Setoguchi, 2008). Although a recent study inferred that the arctic–alpine plant Kalmia procumbens colonized central Japan from Beringia during the last glacial period (Ikeda et al., 2017), other studies have not addressed whether Japanese lineages of alpine plants were derived from lineages occurring in Beringia or vice versa. Recent phylogeographic studies have revealed that populations of several alpine plants exhibited high genetic similarity and low genetic diversity across extensive ranges in the northern Pacific region including northern Japan (Hata et al., 2017; Ikeda et al., 2014, 2017; Ikeda, Yakubov, Barkalov, & Setoguchi, 2018).…”

“…Although a recent study inferred that the arctic–alpine plant Kalmia procumbens colonized central Japan from Beringia during the last glacial period (Ikeda et al., 2017), other studies have not addressed whether Japanese lineages of alpine plants were derived from lineages occurring in Beringia or vice versa. Recent phylogeographic studies have revealed that populations of several alpine plants exhibited high genetic similarity and low genetic diversity across extensive ranges in the northern Pacific region including northern Japan (Hata et al., 2017; Ikeda et al., 2014, 2017; Ikeda, Yakubov, Barkalov, & Setoguchi, 2018). These patterns can be explained by recent range expansion across the northern Pacific region from the Kamchatka Peninsula, which is a part of Beringia.…”