High-Throughput Sequencing of 5S-IGS rDNA in Fagus L. (Fagaceae) reveals complex evolutionary patterns and hybrid origin of modern species

Standard models of speciation assume strictly dichotomous genealogies in which a species, the ancestor, is replaced by two offspring species. The reality is more complex: plant species can evolve from other species via isolation when genetic drift exceeds gene flow; lineage mixing can give rise to new species (hybrid taxa such as nothospecies and allopolyploids). The multi-copy, potentially multi-locus 5S rDNA is one of few gene regions conserving signal from dichotomous and reticulate evolutionary processes down to the level of intra-genomic recombination. Here, we provide the first high-throughput sequencing (HTS) 5S intergenic spacer (5S-IGS) data for a lineage of wind-pollinated subtropical to temperate trees, the Fagus crenata – F. sylvatica s.l. lineage, and its distant relative F. japonica. The observed 4,963 unique 5S-IGS variants reflect a long history of repeated incomplete lineage sorting and lineage mixing since the early Cenozoic of two or more paralogous-homoeologous 5S rDNA lineages. Extant species of Fagus are genetic mosaics and, at least to some part, of hybrid origin.The evolution of extra-tropical tree genera involves dynamic speciation processes. High-throughput sequencing data of the multi-copy, potentially multi-locus 5S rDNA reveal a complex history of hybrid origins, lineage sorting and mixing, and intra-genomic competition between paralogous-homeologous loci in the core group of Eurasian beech trees (genus Fagus) and their distant relative, F. japonica. The modern species are genetic mosaics and represent a striking case of at least 35 million years of ongoing reticulate evolution.