Tracing Scots Pine Expansion in Europe Using Patterns of Rare Alleles

Past climatic oscillations have likely played a key role in the evolution of all tree species in Europe, by causing alternating phases of range expansions and population declines. Nevertheless, tree species display remarkable variation in terms of spatial differentiation and levels of genetic diversity, suggesting that other factors have played an important part. Among wind-pollinated trees, Pinus sylvestris displays an extremely low level of genetic structure over most of its distribution, but little is known about how this pattern has emerged. To better understand the processes that shaped this pattern of genetic diversity in P. sylvestris, we analyzed 11,020 SNPs from the nuclear and organellar genomes, sequenced from 185 trees across 20 populations from Europe, including the southern glacial refugia. We find that European populations as far west as France share most of their ancestry with southern populations from the Carpathian region. Populations from southwest Europe represent a second distinct gene pool, and populations from Italy a third. The variation in chloroplast and mitochondrial genomes highlights the importance of pollen dispersal in homogenizing genetic diversity over long distances. The population differentiation in the nuclear and organellar genomes is unlikely to be at drift migration equilibrium as suggested by our analysis of rare alleles. Finally, we found stronger and earlier demographic expansions in populations from the Carpathian region compared to Italy or southwest Europe. Overall, our study highlights the importance of topography and dispersal and the timing of demographic events in the evolution of a wind-pollinated tree while illustrating the benefits of combining marker types and allele rarity to uncover fine levels of genetic structure.