Spatio-temporal evolution of shrub willows (Salix subgenus Vetrix clade) on a global scale

The spatio-temporal evolution of woody plant lineages in the Holarctic is still understudied, limiting our understanding of evolutionary processes that promote higher diversity at higher latitudes in some lineages, which contradicts the latitudinal gradient hypothesis which predicts higher species richness in the tropics. Shrub willows (Salix subgenus Vetrix) comprise about 350 species of which many are adapted to arctic-alpine ecosystems and thus form an important element across the Holarctic region. In this study, we utilized RAD sequencing to estimate the spatio-temporal evolution of the Vetrix clade based on about 140 species covering most of its morphological and geographical diversity. The resolved phylogeny revealed four lineages: the Pan-Himalayan clade, the North American clade and two clades containing species from Eurasia. Widespread circumpolar species form a hybridogenetic grade between the Eurasian and North American clades. Our results confirm that shrub willows originated in the Tertiary, probably in Asia, and that diversification coincided with the climatic cooling in the Pleistocene. At least two radiations were observed, in the Pan Himalayas and in North America. Speciation was further shaped by migration and dispersal in Eurasia, likely accelerated by the uplift of mountain chains, the closure of the Turgai Strait and expansion of suitable habitats. The dated phylogeny revealed that speciation of arctic lineages predates adaptation to high latitudes, as also evident from the fossil record. Small wind-dispersed seeds enabled shrub willows to colonize the expanding arctic tundra regions in the Miocene and their recolonization after the LGM. Given the high observed number of polyploid species equally distributed in all clades and indications of genetic admixture, we assume that species diversity in shrub willows was additionally increased by hybridization and polyploidization.