Novel Arctic colonization origin of the Arctic lineage in Phyllodoce (Ericaceae)

The Arctic flora is widely considered evolutionarily young, reflecting the emergence of unprecedentedly cold environments during the late Pliocene-early Pleistocene transition. Although many Arctic plants are thought to be derived from temperate alpine ancestors, the historical relationship between high-latitude occupancy and lineage divergence remains unclear. Specifically, it remains unclear whether Arctic lineages originated from ancestors that already occupied high-latitude regions before the Arctic environment formed or originated through colonization after the Arctic environment was established. To address this question, we test demographic models associated with the divergence of the Arctic subgenus Eu-Phyllodoce and its sister alpine subgenus (Parabryanthus) within Phyllodoce (Ericaceae).

Whole-genome data from Phyllodoce were used to infer phylogenetic relationships and demographic history. Demographic parameters were estimated in an isolation-with-migration model and evaluated using log-likelihood ratio tests. Historical demographic trajectories were additionally reconstructed using the pairwise sequentially Markovian coalescent (PSMC).

Demographic inference recovered a smaller ancestral effective population size for Eu-Phyllodoce than for Parabryanthus, indicating disproportional retention of ancestral polymorphism. PSMC further showed pronounced demographic expansion in Eu-Phyllodoce following divergence of ancestral lineages, consistent with a strong founder effect in the Arctic lineage. These results are consistent with the scenario that Eu-Phyllodoce originated through novel Arctic colonization.

Our findings support the view that many Arctic plant lineages are evolutionarily young and highlight the roles of climatic cooling during the late Pliocene-early Pleistocene and of novel Arctic colonization in shaping the assembly of the extant Arctic flora.