Incomplete lineage sorting and gene flow within Allium (Amayllidaceae)

Abstract

The phylogeny and systematics of the genus Allium have been studied with a variety of diverse data types, including an increasing amount of molecular data. However, strong phylogenetic discordance and high levels of uncertainty have prevented the identification of a consistent phylogeny. The difficulty in establishing phylogenetic consensus and evidence for genealogical discordance make Allium a compelling test case to assess the relative contribution of incomplete lineage sorting (ILS), gene flow and gene tree estimation error on phylogenetic reconstruction. In this study, we obtained 75 transcriptomes of 38 Allium species across 10 subgenera. Whole plastid genome, single copy genes and consensus CDS were generated to estimate phylogenetic trees both using coalescence and concatenation methods. Multiple approaches including coalescence simulation, quartet sampling, reticulate network inference, sequence simulation, theta of ILS and reticulation index were carried out across the CDS gene trees to investigate the degrees of ILS, gene flow and gene tree estimation error. Afterward, a regression analysis was used to test the relative contributions of each of these forms of uncertainty to the final phylogeny. Despite extensive topological discordance among gene trees, we found a fully supported species tree that agrees with the most of well-accepted relationships and establishes monophyly of the genus Allium. We presented clear evidence for substantial ILS across the phylogeny of Allium. Further, we identified two ancient hybridization events for the formation of the second evolutionary line and subg. Butomissa as well as several introgression events between recently diverged species. Our regression analysis revealed that gene tree inference error and gene flow were the two most dominant factors explaining for the overall gene tree variation, with the difficulty in disentangling the effects of ILS and gene tree estimation error due to a positive correlation between them. Based on our efforts to mitigate the methodological errors in reconstructing trees, we believed ILS and gene flow are two principal reasons for the oft-reported phylogenetic heterogeneity of Allium. This study presents a strongly-supported and well-resolved phylogenetic backbone for the sampled Allium species, and exemplifies how to untangle heterogeneity in phylogenetic signal and reconstruct the true evolutionary history of the target taxa.