Unravelling Complex Hybrid and Polyploid Evolutionary Relationships Using Phylogenetic Placement of Homologous Gene Copies from Target Enrichment Data

Abstract Phylogenomic data sets comprising hundreds of genes have become the standard for plant systematics and phylogenetics. However, large-scale phylogenomic studies often exclude polyploids and hybrids due to the challenges in assessing the origin of duplicated loci and incorporating them into tree reconstruction methods. Using a newly generated target enrichment data set of 1081 genes from 452 samples from the Brassicaceae tribe Arabideae, including many hybrid and high ploidy taxa, we developed a novel approach to disentangle the evolutionary history of this phylogenetically and taxonomically challenging clade. Our approach extends beyond commonly used gene tree-species tree reconciliation techniques by using phylogenetic placement, a method adopted from metagenomics, of gene copies into a diploid tree. We show how it allows for the simultaneous assessment of the origins of ancient and recent hybrids and autopolyploids, and the detection of nested polyploidization events. Additionally, we demonstrate how synonymous substitution rates provide further evidence for the mode of polyploidization, specifically to distinguish between allo- and autopolyploidization, and to identify hybridization events involving a ghost lineage. Our approach can serve as an exploratory tool for large and complex phylogenomic data sets and can aid in identifying polyploid and hybrid clades for further analysis with specialized methods.