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5S-IGS rDNA in wind-pollinated trees ( Fagus L.) encapsulates 55 million years of reticulate evolution and hybrid origins of modern species

By Simone Cardoni, Roberta Piredda, Thomas Denk, Guido W. Grimm, Aristotelis C. Papageorgiou, Ernst-Detlef Schulze, Anna Scoppola, Parvin S. Shanjani, Yoshihisa Suyama, Nobuhiro Tomaru, James Raymond Peter WORTH, Marco Cosimo Simeone

Posted 27 Feb 2021
bioRxiv DOI: 10.1101/2021.02.26.433057

Standard models of plant speciation assume strictly dichotomous genealogies in which a species, the ancestor, is replaced by two offspring species. The reality in wind-pollinated trees with long evolutionary histories is more complex: species evolve from other species through 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. Therefore, it can provide unique insights into the dynamic speciation processes of lineages that diversified tens of millions of years ago. Here, we provide the first high-throughput sequencing (HTS) of the 5S intergenic spacers (5S-IGS) 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 complex history of hybrid origins, lineage sorting, mixing via secondary gene flow, and intra-genomic competition between two or more paralogous-homoeologous 5S rDNA lineages. We show that modern species are genetic mosaics and represent a striking case of ongoing reticulate evolution during the past 55 million years.

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