Evolutionary history of the Arctic flora

The Arctic occupies ~7.11 million km2, about 5% of Earth’s land surface, and is a key component of the global climate system. It has warmed 3–4 times faster than the global average over the past 50 years, and its treeless tundra biome harbors distinctive, cold-adapted biotas. Despite its ecological importance and sensitivity to ongoing warming, the assembly history of the Arctic flora remains poorly understood. Paleoenvironmental evidence indicates dramatic climatic transitions from warm, ice-free conditions in the Eocene to global cooling since the Eocene/Oligocene transition, with tundra vegetation developing by ~3–2 Ma. Molecular studies, however, suggest that ancestors of some Arctic lineages originated in the mid to late Miocene, though most prior work has focused on single taxa and often lacked divergence time estimates or model-based reconstructions. Community assembly mechanisms—immigration, in situ speciation, and extinction—likely shaped the Arctic flora, but the timing and relative contributions of dispersal into the Arctic versus in situ diversification through time remain unclear. This study aims to determine when the modern Arctic flora began to assemble, to test whether dispersal and in situ diversification share similar temporal trends, and to evaluate geological and climatic drivers underlying these dynamics using a multi-clade phylogenetic framework across the angiosperm tree of life.

Previous phylogenetic and phylogeographic studies indicate that many Arctic plants derive from ancestral lineages in high mountains and adjacent southern regions, with evidence for both immigration and in situ speciation contributing to Arctic diversity. However, many such studies have been limited to single genera or lineages, often without robust divergence time estimates or formal ancestral range reconstructions, hindering inference of colonization dynamics through time. Paleobotanical and paleoenvironmental reconstructions document a transition from Eocene broad-leaved evergreen forests to coniferous forests in cooler intervals, with a warm, ice-free middle Eocene Arctic, followed by substantial global cooling after ~34 Ma and particularly after the Middle Miocene Climatic Optimum (~17–14 Ma). Macrofossils suggest that tundra emerged at the end of the Neogene or earliest Pleistocene (~3–2 Ma), whereas molecular evidence points to older, Miocene origins for some Arctic clades. This discrepancy underscores the need for broad, multi-taxon temporal and biogeographic analyses to resolve the assembly timeline and sources of the Arctic flora.

Study design and sampling: The authors selected 32 angiosperm clades spanning 10 orders and 16 families, comprising 3626 species (548 Arctic-distributed, 40 Arctic endemics), to represent the taxonomic, geographic, and ecological diversity of the Arctic flora. DNA sequences were generated in this study or obtained from GenBank. Total genomic DNA was extracted from silica-dried leaves or herbarium specimens; PCR products (primers listed in Supplementary Table 5) were purified and Sanger sequenced. Phylogenetic inference and dating: Per clade, loci were aligned with MAFFT v7 and manually adjusted in Geneious. Conflicting taxa between plastid and nuclear trees were identified via ML analyses in IQ-TREE v2.1.2; 68 non-Arctic taxa with strong topological conflict (>70% bootstrap) were removed, yielding 3588 species for final analyses. Time-calibrated phylogenies were inferred in BEAST v1.8.4 using uncorrelated relaxed clocks, a Yule prior, and GTR+I+Γ models per locus. Analyses ran for 50 million generations, sampling every 5000, with convergence assessed in Tracer (ESS > 200). Fossils or secondary calibrations were applied as available for each clade. Biogeography and habitat: Ancestral ranges were reconstructed for each clade in BioGeoBEARS under the DEC model. To incorporate phylogenetic uncertainty, 1000 posterior trees from BEAST were sampled, with MCC trees used as representatives. Species were categorized as Arctic (north of the natural tree line), non-Arctic, or occurring in both. The authors compiled credibility intervals for dispersal into the Arctic and in situ diversification within the Arctic, and calculated maximal numbers of observed events per million years (MDEs) through time to characterize temporal dynamics. Habitat ancestral state reconstructions were performed to test whether Arctic immigrants were pre-adapted to open, cold habitats versus undergoing habitat shifts. Biogeographic analyses employed 13 predefined geographic regions to infer source areas and dispersal pathways.

• Identified 131 Arctic-related biogeographic events across 32 clades: 105 dispersal events into the Arctic and 26 in situ diversification events. Dispersal events outnumber in situ events by ~4:1, indicating immigrants dominate current Arctic angiosperm diversity.
• Temporal dynamics (MDE analyses) show concordant trends for dispersal and in situ diversification: initiation in the early Late Miocene (~10–9 Ma), rapid increase around 2.6 Ma, and peaks at ~0.73 Ma (dispersal; 95% CI 0.90–0.60) and ~1.0 Ma (in situ; 95% CI 1.10–0.60). Change points support stepwise assembly: for dispersal at 7.23, 2.56, 0.63 Ma; for in situ diversification at 6.25, 2.34, 0.68 Ma.
• Earliest dispersals into the Arctic date to ~10.2 Ma (95% CI 10.5–9.1), including Artemisia (from the Mediterranean) and Pleuropogon (from western North America). Earliest in situ diversification dates to ~9.2 Ma (95% CI 10.1–6.0) in Artemisia, Puccinellia, and Ranunculus.
• Mean crown ages: sampled Arctic species ~2.66 Ma; sampled Arctic endemics ~1.60 Ma.
• Habitat reconstructions indicate Arctic immigrants (especially endemics) derive from ancestors inhabiting open, cold habitats in southern high mountains and adjacent lowlands, suggesting niche conservatism and pre-adaptation rather than substantial habitat shifts.
• Source regions: Arctic species are derived from multiple regions, with western North America contributing the largest share (~54% of dispersal events). MDEs of dispersal from western North America, Europe, and Asia show similar temporal patterns.
• Evidence for a long-term dispersal corridor between the Arctic and western North America, with interchanges throughout the assembly process.
• Declines in both dispersal and in situ diversification rates after ~0.7 Ma coincide with intensified glacial cycles (~100-ky pacing) and extreme cooling, potentially limiting colonization and increasing extinction.
• Temporal patterns align with geologic and climatic drivers: increased canopy openness beginning ~9.7 Ma; uplift in Alaska and Greenland and onset of Northern Hemisphere glaciation ~7–6 Ma; transition to Icehouse state and large-scale glaciation beginning ~2.6 Ma; high-frequency sea-level oscillations and glacial dynamics between ~2.5–1 Ma promoting habitat diversification and isolation.

The study addresses when and how the Arctic angiosperm flora assembled by integrating multi-clade, time-calibrated phylogenies with biogeographic and habitat reconstructions. Results show that both immigration and in situ speciation began in the early Late Miocene and followed parallel, stepwise temporal trajectories, with sharp increases around the Pliocene–Pleistocene transition and peaks near 1.0–0.7 Ma. These dynamics correspond to progressive Arctic landscape evolution (uplift, erosion, increasing topographic relief), increasing canopy openness, and global climatic deterioration, including the onset and intensification of Northern Hemisphere glaciation and frequent sea-level fluctuations. The concordance suggests that geological and climatic processes jointly facilitated colonization, ecological opportunity, and diversification via increased habitat heterogeneity, local adaptation, and isolation. Habitat ancestral reconstructions indicate that many Arctic immigrants were pre-adapted to open, cold environments, supporting niche conservatism in Arctic lineages. Biogeographic analyses highlight western North America as a predominant source and reveal a persistent dispersal corridor between western North America and the Arctic throughout the assembly process. After ~0.7 Ma, both dispersal and in situ diversification declined, likely reflecting heightened climatic extremes and stronger ~100-ky glacial cycles that constrained colonization and elevated extinction risk. Together, the findings reconcile fossil- and molecule-based timelines by showing Miocene initiation but major Quaternary expansion, offering a unified, stepwise model of Arctic flora assembly.

This multi-taxon phylogenetic and biogeographic study demonstrates that the Arctic angiosperm flora assembled via both long-term dispersal and in situ diversification, beginning in the early Late Miocene and intensifying through the Pliocene–Pleistocene in response to landscape evolution, global cooling, and sea-level fluctuations. Arctic immigrants predominantly originated from open, cold habitats in southern high mountains and adjacent lowlands, with western North America serving as a major, long-term source region linked by a persistent dispersal corridor. The stepwise assembly model and identification of key source–sink dynamics have important conservation implications for safeguarding the unique and fragile Arctic flora, including prioritizing the inferred dispersal corridor between the Arctic and western North America.

Although this study is the most comprehensive evolutionary analysis of the Arctic tundra flora to date, it samples about 26% of Arctic angiosperm diversity. Inferences rely on molecular dating, model-based ancestral range and habitat reconstructions, and analyses across predefined regions; broader taxonomic sampling and additional data could refine timelines and source-area estimates.