Unravelling complex hybrid and polyploid evolutionary relationships using phylogenetic placement of paralogs from target enrichment data

Phylogenomic datasets 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 paralog status of targeted loci and incorporating them into tree reconstruction methods. Using a target enrichment dataset 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 paralogous sequences into a diploid tree. We call this approach Paralog PhyloGenomics (PPG), and 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 will be a valuable addition to phylogenomic methods available for the study of polyploids.