Phylogenomic insights into incomplete lineage sorting and hybridization in early-diverging eudicots

Abstract

The rise of angiosperms has been regarded as a trigger for the Cretaceous Terrestrial Revolution (KTR). The well-defined clade of eudicots contains 75% of all angiosperm species. However, the order- and family-level relationships among early-diverging eudicot lineages (i.e., Ranunculales, Proteales, Trochodendrales, and Buxales), including the sister group relationship of core eudicots and the positions of Sabiaceae and Eupteleaceae remain controversial. Here, we present phylogenetic analyses of early-diverging eudicots (16 species from 16 genera representing all 13 families) based on nuclear and plastid genomic data. We reconstructed the phylogenetic relationships within early-diverging eudicots using concatenated and coalescent approaches. We performed divergence time estimation, gene tree discordance analysis, incomplete lineage sorting assessment, and phylogenetic network inference. Our results show that nuclear and plastid genomic data generated congruent topologies, but different methods recovered different lineage as sister to core eudicots. The species trees support the Trochodendrales-Buxales clade as sister to core eudicots, while the concatenated trees support Trochodendrales and Buxales as successive sisters to core eudicots. Within eudicots, Ranunculales is the earliest-diverging lineage, followed by Proteales. Eupteleaceae is the earliest-diverging lineage in Ranunculales, followed by Papaveraceae. Sabiaceae is sister to the remaining Proteales. Widespread discordance across nuclear gene trees was observed. We detected substantial incomplete lineage sortings across early-diverging eudicots and identified four potential hybridizations involving Ranunculales, Proteales, and core eudicots. The incomplete lineage sorting is likely the primary source of phylogenetic conflicts among early-diverging eudicots, although hybridization cannot be omitted. The eudicots became differentiated in the Lower Cretaceous and all thirteen families of early-diverging eudicots might have emerged by the Lower-Mid Cretaceous, temporally in agreement with the KTR. Incomplete lineage sorting and hybridization occurred during the early rapid diversification of eudicots might be associated with past environmental changes. These findings shed light on the evolutionary history of early-diverging eudicots, and highlight the roles of incomplete lineage sorting and hybridization in the rapid expansion of angiosperms during the KTR.