Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition.

Abstract

The transition of traits between genetically related lineages is a fascinating topic that provides clues to understanding the drivers of speciation and diversification. Much can be learned about this process from phylogeny-based trait evolution. However, such inference is often plagued by genome-wide gene-tree discordance (GTD), mostly due to incomplete lineage sorting (ILS) and/or introgressive hybridization, especially when the genes underlying the traits appear discordant. Here, by collecting transcriptomes, whole chloroplast genomes (cpDNA), and population genetic datasets, we used the coalescent model to turn GTD into a source of information for ILS and employed hemiplasy to explain specific cases of apparent "phylogenetic discordance" between different morphological traits and probable species phylogeny in the Allium subg. Cyathophora. Both concatenation and coalescence methods consistently showed the same phylogenetic topology for species tree inference based on single-copy genes (SCGs), as supported by the K_S distribution. However, GTD was high across the genomes of subg. Cyathophora: ∼27%-38.9% of the SCG trees were in conflict with the species tree. Plasmid and nuclear incongruence was also present. Our coalescent simulations indicated that such GTD was mainly a product of ILS. Our hemiplasy risk factor calculations supported that random fixation of ancient polymorphisms in different populations during successive speciation events along the subg. Cyathophora phylogeny may have caused the character transition, as well as the anomalous cpDNA tree. Our study exemplifies how phylogenetic noise can be transformed into evolutionary information for understanding character state transitions along species phylogenies.