Divergence amid recurring gene flow: complex demographic histories for two North American pine species (Pinus pungens and P. rigida) fit growing expectations among forest trees

Long-lived species of trees, especially conifers, often display weak patterns of reproductive isolation, but clear patterns of local adaptation and phenotypic divergence. Discovering the evolutionary history of these patterns is paramount to a generalized understanding of speciation for long-lived plants. We focus on two closely related yet phenotypically divergent pine species, Pinus pungens and P. rigida, that co-exist along high elevation ridgelines of the southern Appalachian Mountains. In this study, we performed historical species distribution modeling (SDM) to form hypotheses related to population size change and gene flow to be tested in a demographic inference framework. We further sought to identify drivers of divergence by associating climate and geographic variables with genetic structure within and across species boundaries. Population structure within each species was absent based on genome-wide RADseq data. Signals of admixture were present range-wide, however, and species-level genetic differences associated with precipitation seasonality and elevation. When combined with information from contemporary and historical species distribution models, these patterns are consistent with a complex evolutionary history of speciation influenced by Quaternary climate. This was confirmed using inferences based on the multidimensional site frequency spectrum, where demographic modeling inferred recurring gene flow since divergence (2.74 million years ago) and population size reductions that occurred during the last glacial period (similar to 35.2 thousand years ago). This suggests that phenotypic and genomic divergence, including the evolution of divergent phenological schedules leading to partial reproductive isolation, as previously documented for these two species, can happen rapidly, even between long-lived species of pines.

Automated summary

Long-lived tree species, particularly conifers, often exhibit weak patterns of reproductive isolation but show clear patterns of local adaptation and phenotypic divergence. Understanding the evolutionary history of these patterns is crucial for a general understanding of speciation in long-lived plants. In this study, we focused on two closely related pine species, Pinus pungens and P. rigida, which coexist in the high elevation ridgelines of the southern Appalachian Mountains. Our findings suggest a complex evolutionary history of speciation influenced by Quaternary climate, with evidence of recurring gene flow and population size reductions during the last glacial period. These results demonstrate that phenotypic and genomic divergence can occur rapidly, even between long-lived species of pines.