Phylogenomic Analyses Reveal Widespread Gene Flow During the Early Radiation of Oaks and Relatives (Fagaceae: Quercoideae)

Abstract

AO_SCPLOWBSTRACTC_SCPLOWOaks (Quercus), one of the most species-rich and ecologically dominant woody plant clades in the Northern Hemisphere, are well known for their propensity to hybridize and form syngameons, complexes where alleles are readily exchanged among closely related species. While hybridization has been extensively studied towards the tips of the oak phylogeny, the extent, timeline, and evolutionary scenarios of hybridization during the early radiation of oaks and related genera (Quercoideae) remain poorly known. Using an expansive new dataset of nuclear and chloroplast sequences (including up to 431 spp.), we conducted a multifaceted phylogenomic investigation of Quercus aimed at characterizing gene-tree and cytonuclear (chloroplast-nuclear) discordance and identifying ancient reticulation in the early evolution of the group. We document extensive nuclear gene-tree and cytonuclear discordance at deep nodes in Quercus and Quercoideae, with Quercus recovered as non-monophyletic in the chloroplast phylogeny. Analyses recovered clear signatures of gene flow against a backdrop of incomplete lineage sorting, with gene flow most prevalent among major lineages of Quercus and Quercoideae during their initial radiation, dated to the early-middle Eocene. Ancestral reconstructions including fossil data suggest that the ancestors of Castanea+Castanopsis, Lithocarpus, and the Old World oak clade co-occurred in North America and Eurasia, while the ancestors of Chrysolepis, Notholithocarpus, and the New World oak clade co-occurred in North America, offering ample opportunity for hybridization in each region. Following this initial phase of radiation and reticulation, we detected multiple niche shifts in Quercus and other Quercoideae genera that likely facilitated their expansion into new habitats arising from post-Eocene climatic changes. Our study shows that hybridization--perhaps in the form of ancient syngameons similar to those seen today--has been a common and important process throughout the evolutionary history of oaks and their close relatives.