Ancient Bottleneck events, natural selection, and increased risk of maladaptation shape the past, present and future population structure of a widespread conifer

Background Demographic events and natural selection can have independent and confounding effects on population structure and adaptation capability. This means different species could have had very different paths to their current population structure. The influences of demography and selection along a species’ evolutionary timeline can influence responses to current and future stressors. We used two genome-wide and range-wide datasets in Ponderosa pine ( Pinus ponderosa ) to better understand the influences of demography and selection on current population structure and future maladaptation risk. Results Samples were sequenced with 55,000 capture-seq probes, producing 1.2-1.5 million SNPs (400Mbp per sample) in each dataset. We examined current population structure, changes in effective population size, evidence for selection, genome-environment associations and future maladaptation risk using genomic offset. We identified four genetic clusters within the species; numerous bottleneck events that mirror glacial advances and past droughts; signatures of purifying and balancing selection; important environmental variables; and many geographic areas with high amounts of genomic offset. Conclusions Differentiation across varieties has mostly been driven by two processes (1) bottleneck events causing random losses of alleles and decreased connectivity, (2) spatially heterogeneous selection and purifying selection in response to varied moisture levels. Many areas are predicted to be at risk of future maladaptation, which coincide with areas showing increased mortality events and decreased regeneration in previous studies. Previous evolutionary events and rapidly changing climate have shaped future maladaptation risk. Drastic changes from current genomic structure are needed to meet a rapidly changing climate.