Serpentine mountain uplift in northern Japan triggered the divergence of a narrow endemic from a widespread (sub)arctic Asia-Alaska species complex ofLagotis(Plantaginaceae)

Abstract

In the circumboreal region, plants often have extremely-wide species ranges. Lagotis minor-glauca species complex widespread from (sub)arctic Asia to Alaska, however, have two allied narrow endemics in northern Japan: a serpentine plant L. takedana endemic to the Yubari Mountains (Mt. Yubari) and a non-serpentine plant L. yesoensis endemic to the Taisetsu Mountains (Mt. Taisetsu). Elucidating their origins sheds light on drivers for secondary-speciation of widespread circumboreal plants. To infer phylogenetic distinctiveness of two narrow endemics with those related taxa, which contained 25 out of all the 29 species of the genus, chloroplast DNA (cpDNA), nuclear ribosomal (nrITS), two low copy nuclear gene (LCN) markers and genome-wide single-nucleotide polymorphism genotyping (MIG-seq) were used. In the result of cpDNA analyses, the Lagotis minor-glauca species complex formed a clade. Within the clade, L. yesoensis and a portion of L. glauca samples formed a subclade. However, monophyly of each of the four species was not supported. In the results of nrITS and two LCN analyses, L. takedana was monophyletic, while monophyly was not recovered for each L. yesoensis, L. glauca, and L. minor. Based on a Bayesian dating analysis using nrITS data, the age of the most recent common ancestor of L. takedana was Ma (95% confidence interval: 0.05-1.75 Ma). Possible scenario is that an ancestral linage being adapted to serpentine soils migrated into the alpine habitat of Mt. Yubari, that was formed with mountain uplift by the early Pleistocene, and subsequently reproductively isolated from non-serpentine populations and speciated. The contrasting result of L. yesoensis, that was phylogenetically indistinct, is possibly explained by incorrect taxonomy, or alternatively, shallow history and incomplete lineage sorting. In Mt. Taisetsu, massive volcanic eruptions had occurred the Early Pleistocene and even after the last glacial period, suggesting that alpine plants have not migrated into and established populations in Mt. Taisetsu until very recently. To fully resolve the phylogeny of the three species L. yesoensis, L. glauca, and L. minor, further analyses using high resolution molecular markers are needed. The present study illustrated that two narrow endemics in northern Japan diverged from the widespread species include phylogenetically distinctive and indistinctive species, owing to historical orogeny and ecological factors.