Abstract
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 (~ 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.
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Acknowledgements
We thank Mitra Menon and Rebecca Piri for their assistance with field sampling, Brandon Lind for providing computational support, and the undergraduate researchers who helped with the DNA extraction protocol: Kaylyn Carver, Casey Harless, and Leslie Ranson. We also thank the VCU Center for High Performance Computing for providing computational resources with which we made demographic inferences.
Funding
This research was funded by Virginia Commonwealth University (VCU) Department of Biology, VCU Integrative Life Sciences, and National Science Foundation (NSF) awards to Andrew J. Eckert (NSF-EF-1442486) and Christopher J. Friedline (NSF-NPGI-PRFB-1306622).
Field sampling permits at National Parks and State Parks were obtained prior to collecting leaf tissue: ACAD-2017-SCI-007, BLRI-2013-SCI-0027, GRSM-2017-SCI-2028, ZZ-RCP-112514, and SFRA-1725.
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CB performed field sampling of Pinus rigida, data analyses, and modeling. TF processed the genetic data and advised statistical analyses. CF led the field sampling and library prep for Pinus pungens, and AJE assisted with data analyses. All authors contributed to the writing of this manuscript.
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Raw reads generated during this study are available at NCBI SRA database under BioProject: PRJNA803632 (Sample IDs: SAMN25684544 – SAMN25684843). Python scripts for demographic modeling and R scripts for genetic analyses and producing SDMs are available at https://doi.org/10.5072/zenodo.1091266.
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Bolte, C.E., Faske, T.M., Friedline, C.J. et al. 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. Tree Genetics & Genomes 18, 35 (2022). https://doi.org/10.1007/s11295-022-01565-8
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DOI: https://doi.org/10.1007/s11295-022-01565-8