Mitochondrial introgression and complex biogeographic history of the genus Picea

Biogeographic history of plants is much more complex in the Northern Hemisphere than in the Southern Hemisphere due to that both the Bering and the North Atlantic land bridges contributed to floristic exchanges in the Cenozoic, which led to hybridization between congeneric species from different continents. It would be interesting to know how intercontinental gene flow and introgression have affected plant phylogenetic reconstruction and biogeographic inference. In this study, we reinvestigated the phylogenetic and biogeographic history of Picea, a main component of the Northern Hemisphere forest with many species that originated from recent radiation, using two chloroplast (cp), one mitochondrial (mt) and three single-copy nuclear gene markers. The generated gene trees are topologically highly discordant and the geographically closely related species generally show a close affinity of mtDNA rather than cp- or nuclear DNA, suggesting that inter- and intra-continental gene flow and mtDNA introgression might have occurred commonly. However, all gene trees resolved Picea breweriana as the basal-most lineage, which, together with fossil evidence, supports the North American origin hypothesis for the genus. Both dispersal and vicariance have played important roles in the evolution of Picea, and the Bering Land Bridge could have mediated the “North America to Eurasia” dispersal at least two times during the Miocene and Pliocene. Our study again demonstrates the importance of applying data from three genomes for a clear understanding of evolutionary histories in the pine family. Any markers from a single genome alone will not reveal a clear picture of the phylogenetic relationships among closely related congeneric species. In particular, mtDNA markers should be cautiously used, considering that introgression of the maternally inherited mtDNA with a lower rate of gene flow (by seeds) could have occurred much more frequently than that of the paternally inherited cpDNA with a higher rate of gene flow (by pollen) in Pinaceae.