The impact of Pleistocene glacial cycles on the evolutionary diversification of the arctic-alpine Silene acaulis species complex

Arctic-alpine species are highly sensitive to long-term temperature changes and associated glacial cycles due to their occurrence in cold environments to which they are adapted and spatially restricted. Unravelling their evolutionary responses to past climatic fluctuations can provide new insights into their diversification. In this study, we investigated the evolutionary history of the Silene acaulis species complex and how it was shaped by past glacial cycles. We assembled the first high-quality reference genome for S. acaulis and analyzed reduced representation sequencing data from 955 individuals spanning 132 populations across the Holarctic distribution range of these arctic-alpine cushion plants. We identified five evolutionary lineages and assessed their phylogeographical structure in relation to current subspecies classifications, refugia, and historic migration patterns. Phylogenetic dating revealed that lineage divergence largely coincided with repeated phases of glacial cooling over the last two million years and was driven by isolation in glacial refugia. Secondary contact in glacial refugia or during interglacial expansions promoted hybridization and further shaped the distribution of genetic diversity across the species complex. Adaptive divergence among sympatric genetic groups in the European Alps highlights the contribution of niche specialization to intraspecific divergence, with evidence for ecotype differentiation in response to a combination of edaphic and climatic factors. The S. acaulis species complex has an intricate evolutionary history, shaped by glacial cycles in the Late Pleistocene that have driven lineage diversification, secondary contact and ecotype formation. Our study underscores the significance of glacial cycles in shaping genetic diversity in arctic-alpine plant species and improves our understanding of how arctic-alpine species have responded to past climate fluctuations.