Whole chloroplast genomes reveal a complex genetic legacy of lost lineages, past radiations and secondary contacts in the dominant temperate deciduous tree genus Fagus

Abstract

Background--Major northern temperate tree genera emerged in the Eocene and now have vast ranges across the Northern Hemisphere. Here we undertake a multi-discipline study to provide novel insights into the formation and biogeographic history of a dominant, yet understudied temperate tree genus, Fagus L. Data and methodology--A whole chloroplast genome phylogeny (eighty-two chloroplast genomes) with multi-accessions of most species was determined and contrasted with the timing of lineage diversification inferred from three different nuclear and chloroplast gene time-calibrated phylogenies using 101 fossils as age priors. Main results--Five deeply diverged chloroplast lineages were revealed that, with the exception of a Eurasian lineage, underwent divergence decoupled from speciation predating modern species lineages by up to 28 million years (Ma). The geographic distribution of chloroplast lineages reflects a complex history of genetic admixture during past contact between extinct and modern species including between different subgenera in East Asia and long-term persistence particularly in Japan which is the hotspot of plastome diversity. Conclusion--Modern Fagus forests are the consequence of 62 million years of evolution, migration, genetic exchange and species extinction with most modern species harbouring a mosaic of genetic material, a legacy of multiple admixture events in deep time.