Phylogenomics of East Asian lineage within subgenus Anguinum (Allium, Amaryllidaceae): insights into its taxonomic puzzles and phylogenetic conflicts.

Phylogenomic data enriched with informative loci have significantly improved phylogenetic resolution and facilitated the elucidation of evolutionary mechanisms underlying phylogenetic discordance. Species of the East Asian lineage (EAL) within the Allium subgenus Anguinum are widespread in the Himalaya-Hengduan Mountains (HHMs), which exhibit long-standing taxonomic ambiguity and phylogenetic discordance, calling for investigation. In this study, we collected 102 samples, including 45 transcriptomes and 57 plastid genomes, covering multiple populations of all currently recognized taxa within the EAL and relatives. A total of 2,186 low-copy nuclear genes (LCGs) and 163 plastid sequences (including 111 genes and 52 intergenic regions) were employed for phylogenetic analyses. Our results revealed that the EAL is a monophyletic taxon but exhibits a polytomous phylogeny, it further divides into four sublineages in the LCG-based tree and two sublineages in the plastid-based tree, which display distinct geographical distribution patterns. Samples of A. ovalifolium var. leuconeurum, A. ovalifolium var. cordifolium and A. funckiifolium from the northwest Sichuan Basin and Qinling-Daba Mountains clustered within the A. ovalifolium samples of these regions, while A. nanodes is entirely embedded within the HHMs populations of A. prattii and A. ovalifolium. Extensive phylogenetic conflicts were detected within EAL, and the ancestral area reconstruction indicates that the EAL originated in the Hengduan Mountains (HDMs). Morphological and phylogenetic evidence confirmed the varietal status of A. ovalifolium var. leuconeurum and A. ovalifolium var. cordifolium, while also proposing the reclassification of A. funckiifolium as A. ovalifolium var. funckiifolium. The observed polytomous phylogeny within EAL is likely attributed to rapid radiations triggered by geological events and climatic fluctuations during the late Pliocene and Pleistocene, coupled with recurrent isolation-contact dynamics, which resulted in the retention of ancestral polymorphisms and historical gene flow. Widespread phylogenetic discordance in the EAL is mainly due to incomplete lineage sorting (ILS), with hybridization also playing key roles. This study not only reveals the underlying causes of taxonomic controversies within the EAL but also provides critical insights into the unique phylogenetic patterns and evolutionary mechanisms shaping plant lineages in the HHMs biodiversity hotspot.