Molecular phylogeny of Anemone (Ranunculaceae), with special emphasis on the origin of alpine species

Abstract

The alpine biome, above the natural tree line, is home to distinctive biotas that can tolerate harsh environmental conditions, and is especially sensitive to the impacts of global warming. However, the actual timeframe during which alpine floras began to appear on a global scale remains unknown. Here, we used Anemone (c. 200 species), an herbaceous plant genus inhabiting a variety of habitats from lowland to high‐alpine zone across multiple continents, to obtain new insights into the historical assembly of this biome. Using nuclear ITS and plastid atpB‐rbcL, trnL‐F, matK, and rbcL sequences, we built a phylogeny that includes 159 individuals of 146 extant Anemone species and 19 outgroups. Within this phylogenetic framework, we estimated divergence times, reconstructed ancestral ranges, and inferred the evolutionary shifts in habitat types. Phylogenetic analyses strongly support the non‐monophyletic Anemone, in which the Clematis‐Anemoclema clade is nested. Two subgenera of Anemone, subg. Anemone and subg. Anemonidium, are strongly supported as monophyletic. Except for Anemone sect. Keiskea, whose Anemone deltoidea is grouped with A. sect. Hepatica, the other seven sections of this genus are monophyletic. Anemone originated in East Asian non‐alpine habitats around 31 Ma, but range expansion and habitat shifts from non‐alpine to alpine mainly occurred after the Miocene Climatic Optimum (c. 14 Ma). The alpine Anemone lineages in different biogeographic regions originated near‐synchronously, beginning in the middle Miocene (c. 16–12 Ma). We also found that the other alpine floristic elements across multiple continents emerged roughly at the same time. Our findings suggest that the rise of global alpine floras is near‐synchronous and began in the middle Miocene, possibly in association with the mid‐Miocene global cooling and regional orogenetic activities. The mid‐late Miocene is an essential period for the assembly and evolution of global alpine floras. The alpine floristic diversity comprises pre‐adapted immigrants from other alpine zones through long‐distance dispersal and descendants from local lowland ancestors, as well as from other regional lowland ancestors to a lesser extent.