Long-distance pollen dispersal during recent colonization favors a rapid but partial recovery of genetic diversity in Picea sitchensis.

Tree species in the northern hemisphere are currently subject to rapid anthropogenic climate change and are shifting their ranges in response. This prompts questions about the mechanisms allowing tree populations to respond quickly to selection pressures when establishing into new areas. Focusing on the northern expanding range edge of Picea sitchensis, a widespread conifer of western North America, we ask how genetic structure and diversity develop during colonization, and assess the role of demographic history in shaping the evolutionary trajectory of an establishing population. We combined 500 yr of tree-ring and genotyping-by-sequencing data in 639 trees at the expansion front on the Kodiak Archipelago. We show that alleles accumulated rapidly during an increase in recruitment rate in the early 1700s. A shift from foreign to local pollen flow subsequently homogenized genetic structure at the expansion front. Taking advantage of the exceptional longevity of conifers, we highlight the major role of long-distance pollen dispersal in the rapid but incomplete recovery of genetic diversity during the initial stages of colonization. We also warn that slow initial population growth as well as long-lasting dominance of local gene flow by early founders could increase evolutionary load under a rapidly changing climate.