Combining mitochondrial and nuclear genome analyses to dissect the effects of colonization, environment, and geography on population structure in Pinus tabuliformis

The phylogeographic histories of plants in East Asia are complex and shaped by both past large-scale climatic oscillations and dramatic tectonic events. The impact of these historic events, as well as ecological adaptation, on the distribution of biodiversity remains to be elucidated. Pinus tabuliformis is the dominant coniferous tree in northern China, with a large distribution across wide environmental gradients. We examined genetic variation in this species using genotyping-by-sequencing and mitochondrial (mt) DNA markers. We found population structure on both nuclear and mt genomes with a geographic pattern that corresponds well with the landscape of northern China. To understand the contributions of environment, geography, and colonization history to the observed population structure, we performed ecological niche modeling and partitioned the among-population genomic variance into isolation by environment (IBE), isolation by distance (IBD), and isolation by colonization (IBC). We used mtDNA, which is transmitted by seeds in pine, to reflect colonization. We found little impact of IBE, IBD, and IBC on variation in neutral SNPs, but significant impact of IBE on a group of outlier loci. The lack of IBC illustrates that the maternal history can be quickly eroded from the nuclear genome by high rates of gene flow. Our results suggest that genomic variation in P. tabuliformis is largely affected by neutral and stochastic processes, and the signature of local adaptation is visible only at robust outlier loci. This study enriches our understanding on the complex evolutionary forces that shape the distribution of genetic variation in plant taxa in northern China, and guides breeding, conservation, and reforestation programs for P. tabuliformis.