Plastid phylogenomic analyses of Fagales reveal signatures of conflict and ancient chloroplast capture

Abstract

Plastid phylogenomic analyses have shed light on many recalcitrant relationships across the angiosperm Tree of Life and continue to play an important role in plant phylogenetics alongside nuclear data sets given the utility of plastomes for revealing ancient and recent introgression. Here we conduct a plastid phylogenomic study of Fagales, aimed at exploring contentious relationships (e.g., the placement of Myricaceae and some intergeneric relationships in Betulaceae, Juglandaceae, and Fagaceae) and dissecting conflicting phylogenetic signals across the plastome. Combining 102 newly sequenced samples with publically available plastomes, we analyzed a dataset including 256 species and 32 of the 34 total genera of Fagales, representing the largest plastome-based study of the order to date. We find strong support for a sister relationship between Myricaceae and Juglandaceae, as well as strongly supported conflicting signal for alternative generic relationships in Betulaceae and Juglandaceae. These conflicts highlight the sensitivity of plastid phylogenomic analyses to genic composition, perhaps due to the prevalence of uninformative loci and heterogeneity in signal across different regions of the plastome. Phylogenetic relationships were geographically structured in subfamily Quercoideae, with Quercus being non-monophyletic and its sections forming clades with co-distributed Old World or New World genera of Quercoideae. Compared against studies based on nuclear genes, these results suggest extensive introgression and chloroplast capture in the early diversification of Quercus and Quercoideae. This study provides a critical plastome perspective on Fagales phylogeny, setting the stage for future studies employing more extensive data from the nuclear genome.